Skip to main content
Microbiological Reviews logoLink to Microbiological Reviews
. 1995 Mar;59(1):124–142. doi: 10.1128/mr.59.1.124-142.1995

The Rhizobium-plant symbiosis.

P van Rhijn 1, J Vanderleyden 1
PMCID: PMC239357  PMID: 7708010

Abstract

Rhizobium, Bradyrhizobium, and Azorhizobium species are able to elicit the formation of unique structures, called nodules, on the roots or stems of the leguminous host. In these nodules, the rhizobia convert atmospheric N2 into ammonia for the plant. To establish this symbiosis, signals are produced early in the interaction between plant and rhizobia and they elicit discrete responses by the two symbiotic partners. First, transcription of the bacterial nodulation (nod) genes is under control of the NodD regulatory protein, which is activated by specific plant signals, flavonoids, present in the root exudates. In return, the nod-encoded enzymes are involved in the synthesis and excretion of specific lipooligosaccharides, which are able to trigger on the host plant the organogenic program leading to the formation of nodules. An overview of the organization, regulation, and function of the nod genes and their participation in the determination of the host specificity is presented.

Full Text

The Full Text of this article is available as a PDF (352.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appelbaum E. R., Thompson D. V., Idler K., Chartrain N. Rhizobium japonicum USDA 191 has two nodD genes that differ in primary structure and function. J Bacteriol. 1988 Jan;170(1):12–20. doi: 10.1128/jb.170.1.12-20.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armitage J. P., Gallagher A., Johnston A. W. Comparison of the chemotactic behaviour of Rhizobium leguminosarum with and without the nodulation plasmid. Mol Microbiol. 1988 Nov;2(6):743–748. doi: 10.1111/j.1365-2958.1988.tb00085.x. [DOI] [PubMed] [Google Scholar]
  3. Atkinson E. M., Long S. R. Homology of Rhizobium meliloti NodC to polysaccharide polymerizing enzymes. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):439–442. doi: 10.1094/mpmi-5-439. [DOI] [PubMed] [Google Scholar]
  4. Atkinson E. M., Palcic M. M., Hindsgaul O., Long S. R. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8418–8422. doi: 10.1073/pnas.91.18.8418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baev N., Endre G., Petrovics G., Banfalvi Z., Kondorosi A. Six nodulation genes of nod box locus 4 in Rhizobium meliloti are involved in nodulation signal production: nodM codes for D-glucosamine synthetase. Mol Gen Genet. 1991 Aug;228(1-2):113–124. doi: 10.1007/BF00282455. [DOI] [PubMed] [Google Scholar]
  6. Baev N., Kondorosi A. Nucleotide sequence of the Rhizobium meliloti nodL gene located in locus n5 of the nod regulon. Plant Mol Biol. 1992 Feb;18(4):843–846. doi: 10.1007/BF00020033. [DOI] [PubMed] [Google Scholar]
  7. Baev N., Schultze M., Barlier I., Ha D. C., Virelizier H., Kondorosi E., Kondorosi A. Rhizobium nodM and nodN genes are common nod genes: nodM encodes functions for efficiency of nod signal production and bacteroid maturation. J Bacteriol. 1992 Dec;174(23):7555–7565. doi: 10.1128/jb.174.23.7555-7565.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Barbour W. M., Hattermann D. R., Stacey G. Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl Environ Microbiol. 1991 Sep;57(9):2635–2639. doi: 10.1128/aem.57.9.2635-2639.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Barnett M. J., Long S. R. DNA sequence and translational product of a new nodulation-regulatory locus: syrM has sequence similarity to NodD proteins. J Bacteriol. 1990 Jul;172(7):3695–3700. doi: 10.1128/jb.172.7.3695-3700.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bec-Ferté M. P., Krishnan H. B., Promé D., Savagnac A., Pueppke S. G., Promé J. C. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257. Biochemistry. 1994 Oct 4;33(39):11782–11788. doi: 10.1021/bi00205a014. [DOI] [PubMed] [Google Scholar]
  11. Bhuvaneswari T. V., Bhagwat A. A., Bauer W. D. Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol. 1981 Nov;68(5):1144–1149. doi: 10.1104/pp.68.5.1144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bibb M. J., Biró S., Motamedi H., Collins J. F., Hutchinson C. R. Analysis of the nucleotide sequence of the Streptomyces glaucescens tcmI genes provides key information about the enzymology of polyketide antibiotic biosynthesis. EMBO J. 1989 Sep;8(9):2727–2736. doi: 10.1002/j.1460-2075.1989.tb08414.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bloemberg G. V., Thomas-Oates J. E., Lugtenberg B. J., Spaink H. P. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol Microbiol. 1994 Feb;11(4):793–804. doi: 10.1111/j.1365-2958.1994.tb00357.x. [DOI] [PubMed] [Google Scholar]
  14. Bohlool B. B., Schmidt E. L. Lectins: a possible basis for specificity in the Rhizobium--legume root nodule symbiosis. Science. 1974 Jul 19;185(4147):269–271. doi: 10.1126/science.185.4147.269. [DOI] [PubMed] [Google Scholar]
  15. Breedveld M. W., Miller K. J. Cyclic beta-glucans of members of the family Rhizobiaceae. Microbiol Rev. 1994 Jun;58(2):145–161. doi: 10.1128/mr.58.2.145-161.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Brewin N. J. Development of the legume root nodule. Annu Rev Cell Biol. 1991;7:191–226. doi: 10.1146/annurev.cb.07.110191.001203. [DOI] [PubMed] [Google Scholar]
  17. Bulawa C. E., Wasco W. Chitin and nodulation. Nature. 1991 Oct 24;353(6346):710–710. doi: 10.1038/353710b0. [DOI] [PubMed] [Google Scholar]
  18. Burn J. E., Hamilton W. D., Wootton J. C., Johnston A. W. Single and multiple mutations affecting properties of the regulatory gene nodD of Rhizobium. Mol Microbiol. 1989 Nov;3(11):1567–1577. doi: 10.1111/j.1365-2958.1989.tb00142.x. [DOI] [PubMed] [Google Scholar]
  19. Caetano-Anollés G., Crist-Estes D. K., Bauer W. D. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J Bacteriol. 1988 Jul;170(7):3164–3169. doi: 10.1128/jb.170.7.3164-3169.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Caetano-Anollés G., Wrobel-Boerner E., Bauer W. D. Growth and Movement of Spot Inoculated Rhizobium meliloti on the Root Surface of Alfalfa. Plant Physiol. 1992 Mar;98(3):1181–1189. doi: 10.1104/pp.98.3.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Carlson R. W., Sanjuan J., Bhat U. R., Glushka J., Spaink H. P., Wijfjes A. H., van Brussel A. A., Stokkermans T. J., Peters N. K., Stacey G. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and II strains of Bradyrhizobium japonicum. J Biol Chem. 1993 Aug 25;268(24):18372–18381. [PubMed] [Google Scholar]
  22. Chua K. Y., Pankhurst C. E., Macdonald P. E., Hopcroft D. H., Jarvis B. D., Scott D. B. Isolation and characterization of transposon Tn5-induced symbiotic mutants of Rhizobium loti. J Bacteriol. 1985 Apr;162(1):335–343. doi: 10.1128/jb.162.1.335-343.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Cooper J. B., Long S. R. Morphogenetic Rescue of Rhizobium meliloti Nodulation Mutants by trans-Zeatin Secretion. Plant Cell. 1994 Feb;6(2):215–225. doi: 10.1105/tpc.6.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Cooper J. E., Rao J. R. Localized Changes in Flavonoid Biosynthesis in Roots of Lotus pedunculatus after Infection by Rhizobium loti. Plant Physiol. 1992 Sep;100(1):444–450. doi: 10.1104/pp.100.1.444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Cren M., Kondorosi A., Kondorosi E. An insertional point mutation inactivates NolR repressor in Rhizobium meliloti 1021. J Bacteriol. 1994 Jan;176(2):518–519. doi: 10.1128/jb.176.2.518-519.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Dakora F. D., Joseph C. M., Phillips D. A. Alfalfa (Medicago sativa L.) Root Exudates Contain Isoflavonoids in the Presence of Rhizobium meliloti. Plant Physiol. 1993 Mar;101(3):819–824. doi: 10.1104/pp.101.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Davis E. O., Evans I. J., Johnston A. W. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol Gen Genet. 1988 Jun;212(3):531–535. doi: 10.1007/BF00330860. [DOI] [PubMed] [Google Scholar]
  28. Davis E. O., Johnston A. W. Analysis of three nodD genes in Rhizobium leguminosarum biovar phaseoli; nodD1 is preceded by noIE, a gene whose product is secreted from the cytoplasm. Mol Microbiol. 1990 Jun;4(6):921–932. doi: 10.1111/j.1365-2958.1990.tb00665.x. [DOI] [PubMed] [Google Scholar]
  29. Davis E. O., Johnston A. W. Regulatory functions of the three nodD genes of Rhizobium leguminosarum biovar phaseoli. Mol Microbiol. 1990 Jun;4(6):933–941. doi: 10.1111/j.1365-2958.1990.tb00666.x. [DOI] [PubMed] [Google Scholar]
  30. Debellé F., Rosenberg C., Dénarié J. The Rhizobium, Bradyrhizobium, and Azorhizobium NodC proteins are homologous to yeast chitin synthases. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):443–446. doi: 10.1094/mpmi-5-443. [DOI] [PubMed] [Google Scholar]
  31. Debellé F., Sharma S. B. Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation. Nucleic Acids Res. 1986 Sep 25;14(18):7453–7472. doi: 10.1093/nar/14.18.7453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Demont N., Ardourel M., Maillet F., Promé D., Ferro M., Promé J. C., Dénarié J. The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (omega-1)-hydroxylated fatty acids. EMBO J. 1994 May 1;13(9):2139–2149. doi: 10.1002/j.1460-2075.1994.tb06490.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Demont N., Debellé F., Aurelle H., Dénarié J., Promé J. C. Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of lipo-oligosaccharidic nodulation factors. J Biol Chem. 1993 Sep 25;268(27):20134–20142. [PubMed] [Google Scholar]
  34. Djordjevic M. A., Redmond J. W., Batley M., Rolfe B. G. Clovers secrete specific phenolic compounds which either stimulate or repress nod gene expression in Rhizobium trifolii. EMBO J. 1987 May;6(5):1173–1179. doi: 10.1002/j.1460-2075.1987.tb02351.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Dockendorff T. C., Sharma A. J., Stacey G. Identification and characterization of the nolYZ genes of Bradyrhizobium japonicum. Mol Plant Microbe Interact. 1994 Mar-Apr;7(2):173–180. doi: 10.1094/mpmi-7-0173. [DOI] [PubMed] [Google Scholar]
  36. Dowling D. N., Broughton W. J. Competition for nodulation of legumes. Annu Rev Microbiol. 1986;40:131–157. doi: 10.1146/annurev.mi.40.100186.001023. [DOI] [PubMed] [Google Scholar]
  37. Downie A. A nod of recognition. Curr Biol. 1991 Dec;1(6):382–384. doi: 10.1016/0960-9822(91)90200-g. [DOI] [PubMed] [Google Scholar]
  38. Downie J. A., Surin B. P. Either of two nod gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum bv viciae. Mol Gen Genet. 1990 Jun;222(1):81–86. doi: 10.1007/BF00283027. [DOI] [PubMed] [Google Scholar]
  39. Downie J. A. The nodL gene from Rhizobium leguminosarum is homologous to the acetyl transferases encoded by lacA and cysE. Mol Microbiol. 1989 Nov;3(11):1649–1651. doi: 10.1111/j.1365-2958.1989.tb00150.x. [DOI] [PubMed] [Google Scholar]
  40. Dénarié J., Cullimore J. Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell. 1993 Sep 24;74(6):951–954. doi: 10.1016/0092-8674(93)90717-5. [DOI] [PubMed] [Google Scholar]
  41. Dénarié J., Debellé F., Rosenberg C. Signaling and host range variation in nodulation. Annu Rev Microbiol. 1992;46:497–531. doi: 10.1146/annurev.mi.46.100192.002433. [DOI] [PubMed] [Google Scholar]
  42. Eardly B. D., Hannaway D. B., Bottomley P. J. Characterization of Rhizobia from Ineffective Alfalfa Nodules: Ability to Nodulate Bean Plants [Phaseolus vulgaris (L.) Savi.]. Appl Environ Microbiol. 1985 Dec;50(6):1422–1427. doi: 10.1128/aem.50.6.1422-1427.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Economou A., Hamilton W. D., Johnston A. W., Downie J. A. The Rhizobium nodulation gene nodO encodes a Ca2(+)-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J. 1990 Feb;9(2):349–354. doi: 10.1002/j.1460-2075.1990.tb08117.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Eskew D. L., Jiang Q., Caetano-Anolles G., Gresshoff P. M. Kinetics of Nodule Development in Glycine soja. Plant Physiol. 1993 Dec;103(4):1139–1145. doi: 10.1104/pp.103.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Evans I. J., Downie J. A. The nodI gene product of Rhizobium leguminosarum is closely related to ATP-binding bacterial transport proteins; nucleotide sequence analysis of the nodI and nodJ genes. Gene. 1986;43(1-2):95–101. doi: 10.1016/0378-1119(86)90012-0. [DOI] [PubMed] [Google Scholar]
  46. Firmin J. L., Wilson K. E., Carlson R. W., Davies A. E., Downie J. A. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol Microbiol. 1993 Oct;10(2):351–360. doi: 10.1111/j.1365-2958.1993.tb01961.x. [DOI] [PubMed] [Google Scholar]
  47. Fisher R. F., Egelhoff T. T., Mulligan J. T., Long S. R. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes Dev. 1988 Mar;2(3):282–293. doi: 10.1101/gad.2.3.282. [DOI] [PubMed] [Google Scholar]
  48. Fisher R. F., Long S. R. Interactions of NodD at the nod Box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J Mol Biol. 1993 Oct 5;233(3):336–348. doi: 10.1006/jmbi.1993.1515. [DOI] [PubMed] [Google Scholar]
  49. Fisher R. F., Long S. R. Rhizobium--plant signal exchange. Nature. 1992 Jun 25;357(6380):655–660. doi: 10.1038/357655a0. [DOI] [PubMed] [Google Scholar]
  50. Fisher R. F., Swanson J. A., Mulligan J. T., Long S. R. Extended Region of Nodulation Genes in Rhizobium meliloti 1021. II. Nucleotide Sequence, Transcription Start Sites and Protein Products. Genetics. 1987 Oct;117(2):191–201. doi: 10.1093/genetics/117.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Franssen H. J., Vijn I., Yang W. C., Bisseling T. Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol Biol. 1992 May;19(1):89–107. doi: 10.1007/BF00015608. [DOI] [PubMed] [Google Scholar]
  52. Geelen D., Mergaert P., Geremia R. A., Goormachtig S., Van Montagu M., Holsters M. Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: evidence that nodS encodes a methyltransferase involved in Nod factor modification. Mol Microbiol. 1993 Jul;9(1):145–154. doi: 10.1111/j.1365-2958.1993.tb01676.x. [DOI] [PubMed] [Google Scholar]
  53. Geiger O., Spaink H. P., Kennedy E. P. Isolation of the Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4'-phosphopantetheine prosthetic group. J Bacteriol. 1991 May;173(9):2872–2878. doi: 10.1128/jb.173.9.2872-2878.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Geiger O., Thomas-Oates J. E., Glushka J., Spaink H. P., Lugtenberg B. J. Phospholipids of Rhizobium contain nodE-determined highly unsaturated fatty acid moieties. J Biol Chem. 1994 Apr 15;269(15):11090–11097. [PubMed] [Google Scholar]
  55. Geremia R. A., Mergaert P., Geelen D., Van Montagu M., Holsters M. The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2669–2673. doi: 10.1073/pnas.91.7.2669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Goethals K., Gao M., Tomekpe K., Van Montagu M., Holsters M. Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: nucleotide sequence and plant-inducible expression. Mol Gen Genet. 1989 Oct;219(1-2):289–298. doi: 10.1007/BF00261190. [DOI] [PubMed] [Google Scholar]
  57. Goethals K., Mergaert P., Gao M., Geelen D., Van Montagu M., Holsters M. Identification of a new inducible nodulation gene in Azorhizobium caulinodans. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):405–411. doi: 10.1094/mpmi-5-405. [DOI] [PubMed] [Google Scholar]
  58. Goethals K., Van Montagu M., Holsters M. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1646–1650. doi: 10.1073/pnas.89.5.1646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Goethals K., Van den Eeede G., Van Montagu M., Holsters M. Identification and characterization of a functional nodD gene in Azorhizobium caulinodans ORS571. J Bacteriol. 1990 May;172(5):2658–2666. doi: 10.1128/jb.172.5.2658-2666.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Graham T. L. Flavonoid and isoflavonoid distribution in developing soybean seedling tissues and in seed and root exudates. Plant Physiol. 1991 Feb;95(2):594–603. doi: 10.1104/pp.95.2.594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Gray J. X., Rolfe B. G. Exopolysaccharide production in Rhizobium and its role in invasion. Mol Microbiol. 1990 Sep;4(9):1425–1431. doi: 10.1111/j.1365-2958.1990.tb02052.x. [DOI] [PubMed] [Google Scholar]
  62. Grob P., Michel P., Hennecke H., Göttfert M. A novel response-regulator is able to suppress the nodulation defect of a Bradyrhizobium japonicum nodW mutant. Mol Gen Genet. 1993 Dec;241(5-6):531–541. doi: 10.1007/BF00279895. [DOI] [PubMed] [Google Scholar]
  63. Gulash M., Ames P., Larosiliere R. C., Bergman K. Rhizobia are attracted to localized sites on legume roots. Appl Environ Microbiol. 1984 Jul;48(1):149–152. doi: 10.1128/aem.48.1.149-152.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Györgypal Z., Kondorosi A. Homology of the ligand-binding regions of Rhizobium symbiotic regulatory protein NodD and vertebrate nuclear receptors. Mol Gen Genet. 1991 Apr;226(1-2):337–340. doi: 10.1007/BF00273624. [DOI] [PubMed] [Google Scholar]
  65. Göttfert M., Grob P., Hennecke H. Proposed regulatory pathway encoded by the nodV and nodW genes, determinants of host specificity in Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2680–2684. doi: 10.1073/pnas.87.7.2680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Göttfert M., Hitz S., Hennecke H. Identification of nodS and nodU, two inducible genes inserted between the Bradyrhizobium japonicum nodYABC and nodIJ genes. Mol Plant Microbe Interact. 1990 Sep-Oct;3(5):308–316. doi: 10.1094/mpmi-3-308. [DOI] [PubMed] [Google Scholar]
  67. Göttfert M., Holzhäuser D., Bäni D., Hennecke H. Structural and functional analysis of two different nodD genes in Bradyrhizobium japonicum USDA110. Mol Plant Microbe Interact. 1992 May-Jun;5(3):257–265. doi: 10.1094/mpmi-5-257. [DOI] [PubMed] [Google Scholar]
  68. Göttfert M., Horvath B., Kondorosi E., Putnoky P., Rodriguez-Quiñones F., Kondorosi A. At least two nodD genes are necessary for efficient nodulation of alfalfa by Rhizobium meliloti. J Mol Biol. 1986 Oct 5;191(3):411–420. doi: 10.1016/0022-2836(86)90136-1. [DOI] [PubMed] [Google Scholar]
  69. Göttfert M., Lamb J. W., Gasser R., Semenza J., Hennecke H. Mutational analysis of the Bradyrhizobium japonicum common nod genes and further nod box-linked genomic DNA regions. Mol Gen Genet. 1989 Feb;215(3):407–415. doi: 10.1007/BF00427037. [DOI] [PubMed] [Google Scholar]
  70. Hamblin J., Kent S. P. Possible role of phytohaemagglutinin in Phaseolus vulgaris L. Nat New Biol. 1973 Sep 5;245(140):28–30. doi: 10.1038/newbio245028a0. [DOI] [PubMed] [Google Scholar]
  71. Hartwig U. A., Maxwell C. A., Joseph C. M., Phillips D. A. Chrysoeriol and Luteolin Released from Alfalfa Seeds Induce nod Genes in Rhizobium meliloti. Plant Physiol. 1990 Jan;92(1):116–122. doi: 10.1104/pp.92.1.116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Hartwig U. A., Maxwell C. A., Joseph C. M., Phillips D. A. Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes. J Bacteriol. 1990 May;172(5):2769–2773. doi: 10.1128/jb.172.5.2769-2773.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Hartwig U. A., Maxwell C. A., Joseph C. M., Phillips D. A. Interactions among Flavonoid nod Gene Inducers Released from Alfalfa Seeds and Roots. Plant Physiol. 1989 Nov;91(3):1138–1142. doi: 10.1104/pp.91.3.1138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Heidstra R., Geurts R., Franssen H., Spaink H. P., Van Kammen A., Bisseling T. Root Hair Deformation Activity of Nodulation Factors and Their Fate on Vicia sativa. Plant Physiol. 1994 Jul;105(3):787–797. doi: 10.1104/pp.105.3.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Henikoff S., Haughn G. W., Calvo J. M., Wallace J. C. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. doi: 10.1073/pnas.85.18.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Hermiller J. B., Tenaglia A. N., Kisslo K. B., Phillips H. R., Bashore T. M., Stack R. S., Davidson C. J. In vivo validation of compensatory enlargement of atherosclerotic coronary arteries. Am J Cardiol. 1993 Mar 15;71(8):665–668. doi: 10.1016/0002-9149(93)91007-5. [DOI] [PubMed] [Google Scholar]
  77. Heron D. S., Pueppke S. G. Mode of infection, nodulation specificity, and indigenous plasmids of 11 fast-growing Rhizobium japonicum strains. J Bacteriol. 1984 Dec;160(3):1061–1066. doi: 10.1128/jb.160.3.1061-1066.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Hirsch A. M., Bhuvaneswari T. V., Torrey J. G., Bisseling T. Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1244–1248. doi: 10.1073/pnas.86.4.1244. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Ho S. C., Schindler M., Wang J. L. Carbohydrate binding activities of Bradyrhizobium japonicum. II. Isolation and characterization of a galactose-specific lectin. J Cell Biol. 1990 Oct;111(4):1639–1643. doi: 10.1083/jcb.111.4.1639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Ho S. C., Wang J. L., Schindler M. Carbohydrate binding activities of Bradyrhizobium japonicum. I. Saccharide-specific inhibition of homotypic and heterotypic adhesion. J Cell Biol. 1990 Oct;111(4):1631–1638. doi: 10.1083/jcb.111.4.1631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Hong G. F., Burn J. E., Johnston A. W. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucleic Acids Res. 1987 Dec 10;15(23):9677–9690. doi: 10.1093/nar/15.23.9677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Honma M. A., Asomaning M., Ausubel F. M. Rhizobium meliloti nodD genes mediate host-specific activation of nodABC. J Bacteriol. 1990 Feb;172(2):901–911. doi: 10.1128/jb.172.2.901-911.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Honma M. A., Ausubel F. M. Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory gene. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8558–8562. doi: 10.1073/pnas.84.23.8558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Horvath B., Bachem C. W., Schell J., Kondorosi A. Host-specific regulation of nodulation genes in Rhizobium is mediated by a plant-signal, interacting with the nodD gene product. EMBO J. 1987 Apr;6(4):841–848. doi: 10.1002/j.1460-2075.1987.tb04829.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Horvath B., Heidstra R., Lados M., Moerman M., Spaink H. P., Promé J. C., van Kammen A., Bisseling T. Lipo-oligosaccharides of Rhizobium induce infection-related early nodulin gene expression in pea root hairs. Plant J. 1993 Oct;4(4):727–733. doi: 10.1046/j.1365-313x.1993.04040727.x. [DOI] [PubMed] [Google Scholar]
  86. Horvath B., Kondorosi E., John M., Schmidt J., Török I., Györgypal Z., Barabas I., Wieneke U., Schell J., Kondorosi A. Organization, structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa. Cell. 1986 Aug 1;46(3):335–343. doi: 10.1016/0092-8674(86)90654-9. [DOI] [PubMed] [Google Scholar]
  87. Hungria M., Joseph C. M., Phillips D. A. Anthocyanidins and Flavonols, Major nod Gene Inducers from Seeds of a Black-Seeded Common Bean (Phaseolus vulgaris L.). Plant Physiol. 1991 Oct;97(2):751–758. doi: 10.1104/pp.97.2.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Hungria M., Joseph C. M., Phillips D. A. Rhizobium nod Gene Inducers Exuded Naturally from Roots of Common Bean (Phaseolus vulgaris L.). Plant Physiol. 1991 Oct;97(2):759–764. doi: 10.1104/pp.97.2.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Jacobs T. W., Egelhoff T. T., Long S. R. Physical and genetic map of a Rhizobium meliloti nodulation gene region and nucleotide sequence of nodC. J Bacteriol. 1985 May;162(2):469–476. doi: 10.1128/jb.162.2.469-476.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. John M., Röhrig H., Schmidt J., Wieneke U., Schell J. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):625–629. doi: 10.1073/pnas.90.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Johnson D., Roth L. E., Stacey G. Immunogold localization of the NodC and NodA proteins of Rhizobium meliloti. J Bacteriol. 1989 Sep;171(9):4583–4588. doi: 10.1128/jb.171.9.4583-4588.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Journet E. P., Pichon M., Dedieu A., de Billy F., Truchet G., Barker D. G. Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J. 1994 Aug;6(2):241–249. doi: 10.1046/j.1365-313x.1994.6020241.x. [DOI] [PubMed] [Google Scholar]
  93. Kape R., Parniske M., Werner D. Chemotaxis and nod Gene Activity of Bradyrhizobium japonicum in Response to Hydroxycinnamic Acids and Isoflavonoids. Appl Environ Microbiol. 1991 Jan;57(1):316–319. doi: 10.1128/aem.57.1.316-319.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Keyser H. H., Bohlool B. B., Hu T. S., Weber D. F. Fast-growing rhizobia isolated from root nodules of soybean. Science. 1982 Mar 26;215(4540):1631–1632. doi: 10.1126/science.215.4540.1631. [DOI] [PubMed] [Google Scholar]
  95. Kijne J. W., Smit G., Díaz C. L., Lugtenberg B. J. Lectin-enhanced accumulation of manganese-limited Rhizobium leguminosarum cells on pea root hair tips. J Bacteriol. 1988 Jul;170(7):2994–3000. doi: 10.1128/jb.170.7.2994-3000.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Kiss G. B., Csanádi G., Kálmán K., Kaló P., Okrész L. Construction of a basic genetic map for alfalfa using RFLP, RAPD, isozyme and morphological markers. Mol Gen Genet. 1993 Apr;238(1-2):129–137. doi: 10.1007/BF00279539. [DOI] [PubMed] [Google Scholar]
  97. Kondorosi E., Buiré M., Cren M., Iyer N., Hoffmann B., Kondorosi A. Involvement of the syrM and nodD3 genes of Rhizobium meliloti in nod gene activation and in optimal nodulation of the plant host. Mol Microbiol. 1991 Dec;5(12):3035–3048. doi: 10.1111/j.1365-2958.1991.tb01863.x. [DOI] [PubMed] [Google Scholar]
  98. Kondorosi E., Gyuris J., Schmidt J., John M., Duda E., Hoffmann B., Schell J., Kondorosi A. Positive and negative control of nod gene expression in Rhizobium meliloti is required for optimal nodulation. EMBO J. 1989 May;8(5):1331–1340. doi: 10.1002/j.1460-2075.1989.tb03513.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Kondorosi E., Pierre M., Cren M., Haumann U., Buiré M., Hoffmann B., Schell J., Kondorosi A. Identification of NolR, a negative transacting factor controlling the nod regulon in Rhizobium meliloti. J Mol Biol. 1991 Dec 20;222(4):885–896. doi: 10.1016/0022-2836(91)90583-r. [DOI] [PubMed] [Google Scholar]
  100. Kosslak R. M., Joshi R. S., Bowen B. A., Paaren H. E., Appelbaum E. R. Strain-Specific Inhibition of nod Gene Induction in Bradyrhizobium japonicum by Flavonoid Compounds. Appl Environ Microbiol. 1990 May;56(5):1333–1341. doi: 10.1128/aem.56.5.1333-1341.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Krishnan H. B., Lewin A., Fellay R., Broughton W. J., Pueppke S. G. Differential expression of nodS accounts for the varied abilities of Rhizobium fredii USDA257 and Rhizobium sp. strain NGR234 to nodulate Leucaena spp. Mol Microbiol. 1992 Nov;6(22):3321–3330. doi: 10.1111/j.1365-2958.1992.tb02200.x. [DOI] [PubMed] [Google Scholar]
  102. Krishnan H. B., Pueppke S. G. nolC, a Rhizobium fredii gene involved in cultivar-specific nodulation of soybean, shares homology with a heat-shock gene. Mol Microbiol. 1991 Mar;5(3):737–745. doi: 10.1111/j.1365-2958.1991.tb00744.x. [DOI] [PubMed] [Google Scholar]
  103. Leigh J. A., Coplin D. L. Exopolysaccharides in plant-bacterial interactions. Annu Rev Microbiol. 1992;46:307–346. doi: 10.1146/annurev.mi.46.100192.001515. [DOI] [PubMed] [Google Scholar]
  104. Leigh J. A., Walker G. C. Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet. 1994 Feb;10(2):63–67. doi: 10.1016/0168-9525(94)90151-1. [DOI] [PubMed] [Google Scholar]
  105. Lerouge P., Roche P., Faucher C., Maillet F., Truchet G., Promé J. C., Dénarié J. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990 Apr 19;344(6268):781–784. doi: 10.1038/344781a0. [DOI] [PubMed] [Google Scholar]
  106. Lewin A., Cervantes E., Chee-Hoong W., Broughton W. J. nodSU, two new nod genes of the broad host range Rhizobium strain NGR234 encode host-specific nodulation of the tropical tree Leucaena leucocephala. Mol Plant Microbe Interact. 1990 Sep-Oct;3(5):317–326. doi: 10.1094/mpmi-3-317. [DOI] [PubMed] [Google Scholar]
  107. Lewis-Henderson W. R., Djordjevic M. A. A cultivar-specific interaction between Rhizobium leguminosarum bv. trifolii and subterranean clover is controlled by nodM, other bacterial cultivar specificity genes, and a single recessive host gene. J Bacteriol. 1991 May;173(9):2791–2799. doi: 10.1128/jb.173.9.2791-2799.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Lewis-Henderson W. R., Djordjevic M. A. nodT, a positively-acting cultivar specificity determinant controlling nodulation of Trifolium subterraneum by Rhizobium leguminosarum biovar trifolii. Plant Mol Biol. 1991 Apr;16(4):515–526. doi: 10.1007/BF00023418. [DOI] [PubMed] [Google Scholar]
  109. Liu Ruilong, Tran Van Mai, Schmidt E. L. Nodulating Competitiveness of a Nonmotile Tn7 Mutant of Bradyrhizobium japonicum in Nonsterile Soil. Appl Environ Microbiol. 1989 Aug;55(8):1895–1900. doi: 10.1128/aem.55.8.1895-1900.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Long S. R. Rhizobium-legume nodulation: life together in the underground. Cell. 1989 Jan 27;56(2):203–214. doi: 10.1016/0092-8674(89)90893-3. [DOI] [PubMed] [Google Scholar]
  111. Luka S., Sanjuan J., Carlson R. W., Stacey G. nolMNO genes of Bradyrhizobium japonicum are co-transcribed with nodYABCSUIJ, and nolO is involved in the synthesis of the lipo-oligosaccharide nodulation signals. J Biol Chem. 1993 Dec 25;268(36):27053–27059. [PubMed] [Google Scholar]
  112. Maillet F., Debellé F., Dénarié J. Role of the nodD and syrM genes in the activation of the regulatory gene nodD3, and of the common and host-specific nod genes of Rhizobium meliloti. Mol Microbiol. 1990 Nov;4(11):1975–1984. doi: 10.1111/j.1365-2958.1990.tb02047.x. [DOI] [PubMed] [Google Scholar]
  113. Marie C., Barny M. A., Downie J. A. Rhizobium leguminosarum has two glucosamine synthases, GlmS and NodM, required for nodulation and development of nitrogen-fixing nodules. Mol Microbiol. 1992 Apr;6(7):843–851. doi: 10.1111/j.1365-2958.1992.tb01535.x. [DOI] [PubMed] [Google Scholar]
  114. Maxwell C. A., Phillips D. A. Concurrent Synthesis and Release of nod-Gene-Inducing Flavonoids from Alfalfa Roots. Plant Physiol. 1990 Aug;93(4):1552–1558. doi: 10.1104/pp.93.4.1552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. McIver J., Djordjevic M. A., Weinman J. J., Bender G. L., Rolfe B. G. 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. 1989 May-Jun;2(3):97–106. doi: 10.1094/mpmi-2-097. [DOI] [PubMed] [Google Scholar]
  116. Meinhardt L. W., Krishnan H. B., Balatti P. A., Pueppke S. G. Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257. Mol Microbiol. 1993 Jul;9(1):17–29. doi: 10.1111/j.1365-2958.1993.tb01665.x. [DOI] [PubMed] [Google Scholar]
  117. Mergaert P., Van Montagu M., Promé J. C., Holsters M. Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1551–1555. doi: 10.1073/pnas.90.4.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Michiels J., De Wilde P., Vanderleyden J. Sequence of the Rhizobium leguminosarum biovar phaseoli syrM gene. Nucleic Acids Res. 1993 Aug 11;21(16):3893–3893. doi: 10.1093/nar/21.16.3893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Mills K. K., Bauer W. D. Rhizobium attachment to clover roots. J Cell Sci Suppl. 1985;2:333–345. doi: 10.1242/jcs.1985.supplement_2.18. [DOI] [PubMed] [Google Scholar]
  120. Mulligan J. T., Long S. R. A family of activator genes regulates expression of Rhizobium meliloti nodulation genes. Genetics. 1989 May;122(1):7–18. doi: 10.1093/genetics/122.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Mulligan J. T., Long S. R. Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc Natl Acad Sci U S A. 1985 Oct;82(19):6609–6613. doi: 10.1073/pnas.82.19.6609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Nap J. P., Bisseling T. Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science. 1990 Nov 16;250(4983):948–954. doi: 10.1126/science.250.4983.948. [DOI] [PubMed] [Google Scholar]
  123. Ndoye I., de Billy F., Vasse J., Dreyfus B., Truchet G. Root nodulation of Sesbania rostrata. J Bacteriol. 1994 Feb;176(4):1060–1068. doi: 10.1128/jb.176.4.1060-1068.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Nieuwkoop A. J., Banfalvi Z., Deshmane N., Gerhold D., Schell M. G., Sirotkin K. M., Stacey G. A locus encoding host range is linked to the common nodulation genes of Bradyrhizobium japonicum. J Bacteriol. 1987 Jun;169(6):2631–2638. doi: 10.1128/jb.169.6.2631-2638.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  126. Peters N. K., Frost J. W., Long S. R. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science. 1986 Aug 29;233(4767):977–980. doi: 10.1126/science.3738520. [DOI] [PubMed] [Google Scholar]
  127. Peters N. K., Long S. R. Alfalfa Root Exudates and Compounds which Promote or Inhibit Induction of Rhizobium meliloti Nodulation Genes. Plant Physiol. 1988 Oct;88(2):396–400. doi: 10.1104/pp.88.2.396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Phillips D. A., Joseph C. M., Maxwell C. A. Trigonelline and Stachydrine Released from Alfalfa Seeds Activate NodD2 Protein in Rhizobium meliloti. Plant Physiol. 1992 Aug;99(4):1526–1531. doi: 10.1104/pp.99.4.1526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Poupot R., Martinez-Romero E., Promé J. C. Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus. Biochemistry. 1993 Oct 5;32(39):10430–10435. doi: 10.1021/bi00090a019. [DOI] [PubMed] [Google Scholar]
  130. Price N. P., Relić B., Talmont F., Lewin A., Promé D., Pueppke S. G., Maillet F., Dénarié J., Promé J. C., Broughton W. J. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol Microbiol. 1992 Dec;6(23):3575–3584. doi: 10.1111/j.1365-2958.1992.tb01793.x. [DOI] [PubMed] [Google Scholar]
  131. Pueppke S. G. Adsorption of slow- and fast-growing rhizobia to soybean and cowpea roots. Plant Physiol. 1984 Aug;75(4):924–928. doi: 10.1104/pp.75.4.924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Recourt K., Schripsema J., Kijne J. W., van Brussel A. A., Lugtenberg B. J. Inoculation of Vicia sativa subsp. nigra roots with Rhizobium leguminosarum biovar viciae results in release of nod gene activating flavanones and chalcones. Plant Mol Biol. 1991 May;16(5):841–852. doi: 10.1007/BF00015076. [DOI] [PubMed] [Google Scholar]
  133. Recourt K., van Brussel A. A., Driessen A. J., Lugtenberg B. J. Accumulation of a nod gene inducer, the flavonoid naringenin, in the cytoplasmic membrane of Rhizobium leguminosarum biovar viciae is caused by the pH-dependent hydrophobicity of naringenin. J Bacteriol. 1989 Aug;171(8):4370–4377. doi: 10.1128/jb.171.8.4370-4377.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  134. Relić B., Perret X., Estrada-García M. T., Kopcinska J., Golinowski W., Krishnan H. B., Pueppke S. G., Broughton W. J. Nod factors of Rhizobium are a key to the legume door. Mol Microbiol. 1994 Jul;13(1):171–178. doi: 10.1111/j.1365-2958.1994.tb00412.x. [DOI] [PubMed] [Google Scholar]
  135. Relić B., Talmont F., Kopcinska J., Golinowski W., Promé J. C., Broughton W. J. Biological activity of Rhizobium sp. NGR234 Nod-factors on Macroptilium atropurpureum. Mol Plant Microbe Interact. 1993 Nov-Dec;6(6):764–774. doi: 10.1094/mpmi-6-764. [DOI] [PubMed] [Google Scholar]
  136. Reuber T. L., Long S., Walker G. C. Regulation of Rhizobium meliloti exo genes in free-living cells and in planta examined by using TnphoA fusions. J Bacteriol. 1991 Jan;173(2):426–434. doi: 10.1128/jb.173.2.426-434.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Reuhs B. L., Carlson R. W., Kim J. S. 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. 1993 Jun;175(11):3570–3580. doi: 10.1128/jb.175.11.3570-3580.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. Roche P., Debellé F., Maillet F., Lerouge P., Faucher C., Truchet G., Dénarié J., Promé J. C. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell. 1991 Dec 20;67(6):1131–1143. doi: 10.1016/0092-8674(91)90290-f. [DOI] [PubMed] [Google Scholar]
  139. Rossen L., Shearman C. A., Johnston A. W., Downie J. A. The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodA,B,C genes. EMBO J. 1985 Dec 16;4(13A):3369–3373. doi: 10.1002/j.1460-2075.1985.tb04092.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  140. Rostas K., Kondorosi E., Horvath B., Simoncsits A., Kondorosi A. Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1757–1761. doi: 10.1073/pnas.83.6.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  141. Rushing B. G., Yelton M. M., Long S. R. Genetic and physical analysis of the nodD3 region of Rhizobium meliloti. Nucleic Acids Res. 1991 Feb 25;19(4):921–927. doi: 10.1093/nar/19.4.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Röhrig H., Schmidt J., Wieneke U., Kondorosi E., Barlier I., Schell J., John M. Biosynthesis of lipooligosaccharide nodulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3122–3126. doi: 10.1073/pnas.91.8.3122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  143. Sadowsky M. J., Cregan P. B., Gottfert M., Sharma A., Gerhold D., Rodriguez-Quinones F., Keyser H. H., Hennecke H., Stacey G. The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):637–641. doi: 10.1073/pnas.88.2.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Sanjuan J., Carlson R. W., Spaink H. P., Bhat U. R., Barbour W. M., Glushka J., Stacey G. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8789–8793. doi: 10.1073/pnas.89.18.8789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Scheres B., Van De Wiel C., Zalensky A., Horvath B., Spaink H., Van Eck H., Zwartkruis F., Wolters A. M., Gloudemans T., Van Kammen A. The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell. 1990 Jan 26;60(2):281–294. doi: 10.1016/0092-8674(90)90743-x. [DOI] [PubMed] [Google Scholar]
  146. Scheu A. K., Economou A., Hong G. F., Ghelani S., Johnston A. W., Downie J. A. Secretion of the Rhizobium leguminosarum nodulation protein NodO by haemolysin-type systems. Mol Microbiol. 1992 Jan;6(2):231–238. doi: 10.1111/j.1365-2958.1992.tb02004.x. [DOI] [PubMed] [Google Scholar]
  147. Schlaman H. R., Horvath B., Vijgenboom E., Okker R. J., Lugtenberg B. J. Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol. 1991 Jul;173(14):4277–4287. doi: 10.1128/jb.173.14.4277-4287.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Schlaman H. R., Lugtenberg B. J., Okker R. J. The NodD protein does not bind to the promoters of inducible nodulation genes in extracts of bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol. 1992 Oct;174(19):6109–6116. doi: 10.1128/jb.174.19.6109-6116.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Schlaman H. R., Okker R. J., Lugtenberg B. J. Regulation of nodulation gene expression by NodD in rhizobia. J Bacteriol. 1992 Aug;174(16):5177–5182. doi: 10.1128/jb.174.16.5177-5182.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Schlaman H. R., Okker R. J., Lugtenberg B. J. Subcellular localization of the Rhizobium leguminosarum nodI gene product. J Bacteriol. 1990 Sep;172(9):5486–5489. doi: 10.1128/jb.172.9.5486-5489.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  151. Schlaman H. R., Spaink H. P., Okker R. J., Lugtenberg B. J. Subcellular localization of the nodD gene product in Rhizobium leguminosarum. J Bacteriol. 1989 Sep;171(9):4686–4693. doi: 10.1128/jb.171.9.4686-4693.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  152. Schofield P. R., Watson J. M. DNA sequence of Rhizobium trifolii nodulation genes reveals a reiterated and potentially regulatory sequence preceding nodABC and nodFE. Nucleic Acids Res. 1986 Apr 11;14(7):2891–2903. doi: 10.1093/nar/14.7.2891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  153. Schultze M., Quiclet-Sire B., Kondorosi E., Virelizer H., Glushka J. N., Endre G., Géro S. D., Kondorosi A. Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):192–196. doi: 10.1073/pnas.89.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  154. Schwedock J., Long S. R. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature. 1990 Dec 13;348(6302):644–647. doi: 10.1038/348644a0. [DOI] [PubMed] [Google Scholar]
  155. Schwedock J., Long S. R. Nucleotide sequence and protein products of two new nodulation genes of Rhizobium meliloti, nodP and nodQ. Mol Plant Microbe Interact. 1989 Jul-Aug;2(4):181–194. doi: 10.1094/mpmi-2-181. [DOI] [PubMed] [Google Scholar]
  156. Scott K. F. Conserved nodulation genes from the non-legume symbiont Bradyrhizobium sp. (Parasponia). Nucleic Acids Res. 1986 Apr 11;14(7):2905–2919. doi: 10.1093/nar/14.7.2905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  157. Sharma S. B., Signer E. R. Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon Tn5-gusA. Genes Dev. 1990 Mar;4(3):344–356. doi: 10.1101/gad.4.3.344. [DOI] [PubMed] [Google Scholar]
  158. Shearman C. A., Rossen L., Johnston A. W., Downie J. A. The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO J. 1986 Apr;5(4):647–652. doi: 10.1002/j.1460-2075.1986.tb04262.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  159. Sheldon P. S., Kekwick R. G., Sidebottom C., Smith C. G., Slabas A. R. 3-Oxoacyl-(acyl-carrier protein) reductase from avocado (Persea americana) fruit mesocarp. Biochem J. 1990 Nov 1;271(3):713–720. doi: 10.1042/bj2710713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  160. Smit G., Kijne J. W., Lugtenberg B. J. Correlation between extracellular fibrils and attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol. 1986 Nov;168(2):821–827. doi: 10.1128/jb.168.2.821-827.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  161. Smit G., Kijne J. W., Lugtenberg B. J. Involvement of both cellulose fibrils and a Ca2+-dependent adhesin in the attachment of Rhizobium leguminosarum to pea root hair tips. J Bacteriol. 1987 Sep;169(9):4294–4301. doi: 10.1128/jb.169.9.4294-4301.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  162. Smit G., Kijne J. W., Lugtenberg B. J. Roles of flagella, lipopolysaccharide, and a Ca2+-dependent cell surface protein in attachment of Rhizobium leguminosarum biovar viciae to pea root hair tips. J Bacteriol. 1989 Jan;171(1):569–572. doi: 10.1128/jb.171.1.569-572.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  163. Smit G., Logman T. J., Boerrigter M. E., Kijne J. W., Lugtenberg B. J. Purification and partial characterization of the Rhizobium leguminosarum biovar viciae Ca2+-dependent adhesin, which mediates the first step in attachment of cells of the family Rhizobiaceae to plant root hair tips. J Bacteriol. 1989 Jul;171(7):4054–4062. doi: 10.1128/jb.171.7.4054-4062.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  164. Smit G., Swart S., Lugtenberg B. J., Kijne J. W. Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol. 1992 Oct;6(20):2897–2903. doi: 10.1111/j.1365-2958.1992.tb01748.x. [DOI] [PubMed] [Google Scholar]
  165. Spaink H. P., Aarts A., Stacey G., Bloemberg G. V., Lugtenberg B. J., Kennedy E. P. Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin-layer chromatography. Mol Plant Microbe Interact. 1992 Jan-Feb;5(1):72–80. doi: 10.1094/mpmi-5-072. [DOI] [PubMed] [Google Scholar]
  166. Spaink H. P., Okker R. J., Wijffelman C. A., Tak T., Goosen-de Roo L., Pees E., van Brussel A. A., Lugtenberg B. J. Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J Bacteriol. 1989 Jul;171(7):4045–4053. doi: 10.1128/jb.171.7.4045-4053.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  167. Spaink H. P. Rhizobial lipo-oligosaccharides: answers and questions. Plant Mol Biol. 1992 Dec;20(5):977–986. doi: 10.1007/BF00027167. [DOI] [PubMed] [Google Scholar]
  168. Spaink H. P., Sheeley D. M., van Brussel A. A., Glushka J., York W. S., Tak T., Geiger O., Kennedy E. P., Reinhold V. N., Lugtenberg B. J. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature. 1991 Nov 14;354(6349):125–130. doi: 10.1038/354125a0. [DOI] [PubMed] [Google Scholar]
  169. Spaink H. P., Weinman J., Djordjevic M. A., Wijffelman C. A., Okker R. J., Lugtenberg B. J. Genetic analysis and cellular localization of the Rhizobium host specificity-determining NodE protein. EMBO J. 1989 Oct;8(10):2811–2818. doi: 10.1002/j.1460-2075.1989.tb08427.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  170. Stacey G., Luka S., Sanjuan J., Banfalvi Z., Nieuwkoop A. J., Chun J. Y., Forsberg L. S., Carlson R. nodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J Bacteriol. 1994 Feb;176(3):620–633. doi: 10.1128/jb.176.3.620-633.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  171. Stokkermans T. J., Peters N. K. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta. 1994;193(3):413–420. doi: 10.1007/BF00201821. [DOI] [PubMed] [Google Scholar]
  172. Surin B. P., Downie J. A. Characterization of the Rhizobium leguminosarum genes nodLMN involved in efficient host-specific nodulation. Mol Microbiol. 1988 Mar;2(2):173–183. doi: 10.1111/j.1365-2958.1988.tb00019.x. [DOI] [PubMed] [Google Scholar]
  173. Surin B. P., Watson J. M., Hamilton W. D., Economou A., Downie J. A. Molecular characterization of the nodulation gene, nodT, from two biovars of Rhizobium leguminosarum. Mol Microbiol. 1990 Feb;4(2):245–252. doi: 10.1111/j.1365-2958.1990.tb00591.x. [DOI] [PubMed] [Google Scholar]
  174. Sutton J. M., Lea E. J., Downie J. A. The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9990–9994. doi: 10.1073/pnas.91.21.9990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  175. Swanson J. A., Mulligan J. T., Long S. R. Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics. 1993 Jun;134(2):435–444. doi: 10.1093/genetics/134.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  176. Toogood C. I., Hay R. T. DNA sequence of the adenovirus type 41 hexon gene and predicted structure of the protein. J Gen Virol. 1988 Sep;69(Pt 9):2291–2301. doi: 10.1099/0022-1317-69-9-2291. [DOI] [PubMed] [Google Scholar]
  177. Trinick M. J. Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can J Microbiol. 1979 May;25(5):565–578. doi: 10.1139/m79-082. [DOI] [PubMed] [Google Scholar]
  178. Tsien H. C., Dreyfus B. L., Schmidt E. L. Initial stages in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J Bacteriol. 1983 Nov;156(2):888–897. doi: 10.1128/jb.156.2.888-897.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  179. Van Brussel A. A., Zaat S. A., Cremers H. C., Wijffelman C. A., Pees E., Tak T., Lugtenberg B. J. Role of plant root exudate and Sym plasmid-localized nodulation genes in the synthesis by Rhizobium leguminosarum of Tsr factor, which causes thick and short roots on common vetch. J Bacteriol. 1986 Feb;165(2):517–522. doi: 10.1128/jb.165.2.517-522.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  180. Vasse J., de Billy F., Camut S., Truchet G. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol. 1990 Aug;172(8):4295–4306. doi: 10.1128/jb.172.8.4295-4306.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  181. Vesper S. J., Bauer W. D. Role of Pili (Fimbriae) in Attachment of Bradyrhizobium japonicum to Soybean Roots. Appl Environ Microbiol. 1986 Jul;52(1):134–141. doi: 10.1128/aem.52.1.134-141.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  182. Vesper S. J., Malik N. S., Bauer W. D. Transposon Mutants of Bradyrhizobium japonicum Altered in Attachment to Host Roots. Appl Environ Microbiol. 1987 Aug;53(8):1959–1961. doi: 10.1128/aem.53.8.1959-1961.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  183. Vázquez M., Dávalos A., de las Peñas A., Sánchez F., Quinto C. Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. J Bacteriol. 1991 Feb;173(3):1250–1258. doi: 10.1128/jb.173.3.1250-1258.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  184. Vázquez M., Santana O., Quinto C. The NodL and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion proteins from gram-negative bacteria. Mol Microbiol. 1993 Apr;8(2):369–377. doi: 10.1111/j.1365-2958.1993.tb01580.x. [DOI] [PubMed] [Google Scholar]
  185. Wang S. P., Stacey G. Ammonia regulation of nod genes in Bradyrhizobium japonicum. Mol Gen Genet. 1990 Sep;223(2):329–331. doi: 10.1007/BF00265071. [DOI] [PubMed] [Google Scholar]
  186. Wang S. P., Stacey G. Studies of the Bradyrhizobium japonicum nodD1 promoter: a repeated structure for the nod box. J Bacteriol. 1991 Jun;173(11):3356–3365. doi: 10.1128/jb.173.11.3356-3365.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  187. Willems A., Collins M. D. Phylogenetic analysis of rhizobia and agrobacteria based on 16S rRNA gene sequences. Int J Syst Bacteriol. 1993 Apr;43(2):305–313. doi: 10.1099/00207713-43-2-305. [DOI] [PubMed] [Google Scholar]
  188. Yanagi M., Yamasato K. Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett. 1993 Feb 15;107(1):115–120. doi: 10.1111/j.1574-6968.1993.tb06014.x. [DOI] [PubMed] [Google Scholar]
  189. Young J. P., Downer H. L., Eardly B. D. Phylogeny of the phototrophic rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol. 1991 Apr;173(7):2271–2277. doi: 10.1128/jb.173.7.2271-2277.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  190. van Brussel A. A., Bakhuizen R., van Spronsen P. C., Spaink H. P., Tak T., Lugtenberg B. J., Kijne J. W. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science. 1992 Jul 3;257(5066):70–72. doi: 10.1126/science.257.5066.70. [DOI] [PubMed] [Google Scholar]
  191. van Brussel A. A., Recourt K., Pees E., Spaink H. P., Tak T., Wijffelman C. A., Kijne J. W., Lugtenberg B. J. A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra. J Bacteriol. 1990 Sep;172(9):5394–5401. doi: 10.1128/jb.172.9.5394-5401.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  192. van Rhijn P. J., Feys B., Verreth C., Vanderleyden J. Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J Bacteriol. 1993 Jan;175(2):438–447. doi: 10.1128/jb.175.2.438-447.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Microbiological Reviews are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES