CoChat
Sign Up
Cited by 692Legume Nitrogen Fixing SymbiosisPlant-Microbe Interactions and ImmunityNematode management and characterization studies

Symbiotic Nitrogen Fixation

Open access
Mylona, P., Pawlowski, K., Bisseling, T.·1995·The Plant Cell
DOI 10.1105/tpc.7.7.869PMC PMC160880
Open this paper in CoChat — free account

Abstract

that are expressed before the onset of nitrogen fixation and are involved in infection and nodule development. The products of the late nodulin genes are involved in the interaction with the endosymbiont and in the metabolic specialization of the nodule (Nap and Bisseling, 1990). In the first part of this review, we describe the early steps of the interaction between rhizobia and legumes that result in the formation of a nitrogen-fixing nodule. We focus on the role of specific lipooligosaccharides secreted by rhizobia in the induction of these early steps. In the second part, we describe nodule functioning and compare actinorhizal and legume nodules.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1105/tpc.7.7.869

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Nitrogen fixers in symbioses with bacteria are able to bind nitrogen from the air and transform it into nitrates, a process which requires nitrogen in the atmosphere.

    “In symbioses with bacteria [12], [13] these nitrogen fixers are able to bind nitrogen from the air and transform it into nitrates, a process which requires nitrogen in the atmosphere.”

    From Can Plants Grow on Mars and the Moon: A Growth Experiment on Mars and Moon Soil Simulants (2014) · cites this paper as [12]

    The indexed copy shows the article title and a reference list, but says the article's full text is available as a PDF; it does not include the article body (article listing, pp. 869–885). Searches for atmospheric nitrogen and conversion to nitrates found no passage in the available copy that addresses the claimed product of fixation, so the decisive text may be missing. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 77

  1. Ardourel M., Demont N., Debellé F., Maillet F., de Billy F., Promé J. C., Dénarié J., Truchet G. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell. 1994 Oct;6(10):1357–1374. doi: 10.1105/tpc.6.10.1357. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  2. Bassett B., Goodman R. N., Novacky A. Ultrastructure of soybean nodules. I: release of rhizobia from the infection thread. Can J Microbiol. 1977 May;23(5):573–582. doi: 10.1139/m77-083. [DOI] [PubMed] [Google Scholar] · DOI
  3. Batut J., Daveran-Mingot M. L., David M., Jacobs J., Garnerone A. M., Kahn D. fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBO J. 1989 Apr;8(4):1279–1286. doi: 10.1002/j.1460-2075.1989.tb03502.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  4. 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] · DOI
  5. Brears T., Walker E. L., Coruzzi G. M. A promoter sequence involved in cell-specific expression of the pea glutamine synthetase GS3A gene in organs of transgenic tobacco and alfalfa. Plant J. 1991 Sep;1(2):235–244. doi: 10.1111/j.1365-313x.1991.00235.x. [DOI] [PubMed] [Google Scholar] · DOI
  6. 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] · DOI
  7. Carlson R. W., Price N. P., Stacey G. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):684–695. doi: 10.1094/mpmi-7-0684. [DOI] [PubMed] [Google Scholar] · DOI
  8. Cook D., Dreyer D., Bonnet D., Howell M., Nony E., VandenBosch K. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell. 1995 Jan;7(1):43–55. doi: 10.1105/tpc.7.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  9. Crespi M. D., Jurkevitch E., Poiret M., d'Aubenton-Carafa Y., Petrovics G., Kondorosi E., Kondorosi A. enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J. 1994 Nov 1;13(21):5099–5112. doi: 10.1002/j.1460-2075.1994.tb06839.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  10. David M., Daveran M. L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell. 1988 Aug 26;54(5):671–683. doi: 10.1016/s0092-8674(88)80012-6. [DOI] [PubMed] [Google Scholar] · DOI
  11. De Jong A. J., Heidstra R., Spaink H. P., Hartog M. V., Meijer E. A., Hendriks T., Schiavo F. L., Terzi M., Bisseling T., Van Kammen A. Rhizobium Lipooligosaccharides Rescue a Carrot Somatic Embryo Mutant. Plant Cell. 1993 Jun;5(6):615–620. doi: 10.1105/tpc.5.6.615. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  12. Dylan T., Ielpi L., Stanfield S., Kashyap L., Douglas C., Yanofsky M., Nester E., Helinski D. R., Ditta G. Rhizobium meliloti genes required for nodule development are related to chromosomal virulence genes in Agrobacterium tumefaciens. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4403–4407. doi: 10.1073/pnas.83.12.4403. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  13. 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] · DOI
  14. Ehrhardt D. W., Atkinson E. M., Long S. R. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science. 1992 May 15;256(5059):998–1000. doi: 10.1126/science.10744524. [DOI] [PubMed] [Google Scholar] · DOI
  15. Forde B. G., Freeman J., Oliver J. E., Pineda M. Nuclear factors interact with conserved A/T-rich elements upstream of a nodule-enhanced glutamine synthetase gene from French bean. Plant Cell. 1990 Sep;2(9):925–939. doi: 10.1105/tpc.2.9.925. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  16. Fortin M. G., Zelechowska M., Verma D. P. Specific targeting of membrane nodulins to the bacteroid-enclosing compartment in soybean nodules. EMBO J. 1985 Dec 1;4(12):3041–3046. doi: 10.1002/j.1460-2075.1985.tb04043.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  17. Gilles-Gonzalez M. A., Ditta G. S., Helinski D. R. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature. 1991 Mar 14;350(6314):170–172. doi: 10.1038/350170a0. [DOI] [PubMed] [Google Scholar] · DOI
  18. Glazebrook J., Ichige A., Walker G. C. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev. 1993 Aug;7(8):1485–1497. doi: 10.1101/gad.7.8.1485. [DOI] [PubMed] [Google Scholar] · DOI
  19. 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] · DOI
  20. Gray J. X., Zhan H. J., Levery S. B., Battisti L., Rolfe B. G., Leigh J. A. Heterologous exopolysaccharide production in Rhizobium sp. strain NGR234 and consequences for nodule development. J Bacteriol. 1991 May;173(10):3066–3077. doi: 10.1128/jb.173.10.3066-3077.1991. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  21. Gussin G. N., Ronson C. W., Ausubel F. M. Regulation of nitrogen fixation genes. Annu Rev Genet. 1986;20:567–591. doi: 10.1146/annurev.ge.20.120186.003031. [DOI] [PubMed] [Google Scholar] · DOI
  22. Hanks J. F., Tolbert N. E., Schubert K. R. Localization of enzymes of ureide biosynthesis in peroxisomes and microsomes of nodules. Plant Physiol. 1981 Jul;68(1):65–69. doi: 10.1104/pp.68.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  23. 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] · DOI
  24. 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] · DOI
  25. Jacobsen-Lyon K., Jensen E. O., Jørgensen J. E., Marcker K. A., Peacock W. J., Dennis E. S. Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell. 1995 Feb;7(2):213–223. doi: 10.1105/tpc.7.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  26. James M. F., van den Berg A. A., French N. A., White J. F. A study of the thermogenic effect of ethanol in the hypothermic rat. Clin Exp Pharmacol Physiol. 1981 Mar-Apr;8(2):119–123. doi: 10.1111/j.1440-1681.1981.tb00142.x. [DOI] [PubMed] [Google Scholar] · DOI
  27. 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] · DOI
  28. Kannenberg E. L., Brewin N. J. Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. J Bacteriol. 1989 Sep;171(9):4543–4548. doi: 10.1128/jb.171.9.4543-4548.1989. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  29. Kardailsky I., Yang W. C., Zalensky A., van Kammen A., Bisseling T. The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENOD3/14 and is expressed after the leghaemoglobin genes. Plant Mol Biol. 1993 Dec;23(5):1029–1037. doi: 10.1007/BF00021817. [DOI] [PubMed] [Google Scholar] · DOI
  30. Kim J., Woo D., Rees D. C. X-ray crystal structure of the nitrogenase molybdenum-iron protein from Clostridium pasteurianum at 3.0-A resolution. Biochemistry. 1993 Jul 20;32(28):7104–7115. doi: 10.1021/bi00079a006. [DOI] [PubMed] [Google Scholar] · DOI
  31. Kouchi H., Hata S. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet. 1993 Apr;238(1-2):106–119. doi: 10.1007/BF00279537. [DOI] [PubMed] [Google Scholar] · DOI
  32. Krey R., Pühler A., Klipp W. A defined amino acid exchange close to the putative nucleotide binding site is responsible for an oxygen-tolerant variant of the Rhizobium meliloti NifA protein. Mol Gen Genet. 1992 Sep;234(3):433–441. doi: 10.1007/BF00538703. [DOI] [PubMed] [Google Scholar] · DOI
  33. Lam H. M., Coschigano K., Schultz C., Melo-Oliveira R., Tjaden G., Oliveira I., Ngai N., Hsieh M. H., Coruzzi G. Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. Plant Cell. 1995 Jul;7(7):887–898. doi: 10.1105/tpc.7.7.887. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  34. 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] · DOI
  35. Marvel D. J., Torrey J. G., Ausubel F. M. Rhizobium symbiotic genes required for nodulation of legume and nonlegume hosts. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1319–1323. doi: 10.1073/pnas.84.5.1319. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  36. Matvienko M., Van de Sande K., Yang W. C., van Kammen A., Bisseling T., Franssen H. Comparison of soybean and pea ENOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Mol Biol. 1994 Oct;26(1):487–493. doi: 10.1007/BF00039559. [DOI] [PubMed] [Google Scholar] · DOI
  37. 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] · DOI
  38. Miao G. H., Hirel B., Marsolier M. C., Ridge R. W., Verma D. P. Ammonia-regulated expression of a soybean gene encoding cytosolic glutamine synthetase in transgenic Lotus corniculatus. Plant Cell. 1991 Jan;3(1):11–22. doi: 10.1105/tpc.3.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  39. Miao G. H., Hong Z., Verma D. P. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. J Cell Biol. 1992 Jul;118(2):481–490. doi: 10.1083/jcb.118.2.481. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  40. Miao G. H., Verma D. P. Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell. 1993 Jul;5(7):781–794. doi: 10.1105/tpc.5.7.781. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  41. Morett E., Buck M. In vivo studies on the interaction of RNA polymerase-sigma 54 with the Klebsiella pneumoniae and Rhizobium meliloti nifH promoters. The role of NifA in the formation of an open promoter complex. J Mol Biol. 1989 Nov 5;210(1):65–77. doi: 10.1016/0022-2836(89)90291-x. [DOI] [PubMed] [Google Scholar] · DOI
  42. Nadler K. D., Avissar Y. J. Heme Synthesis in Soybean Root Nodules: I. On the Role of Bacteroid delta-Aminolevulinic Acid Synthase and delta-Aminolevulinic Acid Dehydrase in the Synthesis of the Heme of Leghemoglobin. Plant Physiol. 1977 Sep;60(3):433–436. doi: 10.1104/pp.60.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  43. 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] · DOI
  44. Nguyen T., Zelechowska M., Foster V., Bergmann H., Verma D. P. Primary structure of the soybean nodulin-35 gene encoding uricase II localized in the peroxisomes of uninfected cells of nodules. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5040–5044. doi: 10.1073/pnas.82.15.5040. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  45. Ouyang L. J., Whelan J., Weaver C. D., Roberts D. M., Day D. A. Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Lett. 1991 Nov 18;293(1-2):188–190. doi: 10.1016/0014-5793(91)81183-9. [DOI] [PubMed] [Google Scholar] · DOI
  46. Pichon M., Journet E. P., Dedieu A., de Billy F., Truchet G., Barker D. G. Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell. 1992 Oct;4(10):1199–1211. doi: 10.1105/tpc.4.10.1199. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  47. 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] · DOI
  48. 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] · DOI
  49. Ramlov K. B., Laursen N. B., Stougaard J., Marcker K. A. Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J. 1993 Sep;4(3):577–580. doi: 10.1046/j.1365-313x.1993.04030577.x. [DOI] [PubMed] [Google Scholar] · DOI
  50. 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] · DOI
  51. 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] · DOI
  52. Ronson C. W., Astwood P. M., Nixon B. T., Ausubel F. M. Deduced products of C4-dicarboxylate transport regulatory genes of Rhizobium leguminosarum are homologous to nitrogen regulatory gene products. Nucleic Acids Res. 1987 Oct 12;15(19):7921–7934. doi: 10.1093/nar/15.19.7921. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  53. Rossbach S., Hennecke H. Identification of glyA as a symbiotically essential gene in Bradyrhizobium japonicum. Mol Microbiol. 1991 Jan;5(1):39–47. doi: 10.1111/j.1365-2958.1991.tb01824.x. [DOI] [PubMed] [Google Scholar] · DOI
  54. 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] · DOI
  55. 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] · DOI
  56. 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] · DOI
  57. Schmitt H. D., Wagner P., Pfaff E., Gallwitz D. The ras-related YPT1 gene product in yeast: a GTP-binding protein that might be involved in microtubule organization. Cell. 1986 Nov 7;47(3):401–412. doi: 10.1016/0092-8674(86)90597-0. [DOI] [PubMed] [Google Scholar] · DOI
  58. Shah V. K., Brill W. J. Isolation of an iron-molybdenum cofactor from nitrogenase. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3249–3253. doi: 10.1073/pnas.74.8.3249. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  59. Soupène E., Foussard M., Boistard P., Truchet G., Batut J. Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3759–3763. doi: 10.1073/pnas.92.9.3759. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  60. 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] · DOI
  61. 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] · DOI
  62. 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] · DOI
  63. 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] · DOI
  64. Szabados L., Ratet P., Grunenberg B., de Bruijn F. J. Functional analysis of the Sesbania rostrata leghemoglobin glb3 gene 5'-upstream region in transgenic Lotus corniculatus and Nicotiana tabacum plants. Plant Cell. 1990 Oct;2(10):973–986. doi: 10.1105/tpc.2.10.973. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  65. Thummler F., Verma D. P. Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules. J Biol Chem. 1987 Oct 25;262(30):14730–14736. [PubMed] [Google Scholar]
  66. 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] · DOI
  67. Verma DPS. Signals in Root Nodule Organogenesis and Endocytosis of Rhizobium. Plant Cell. 1992 Apr;4(4):373–382. doi: 10.1105/tpc.4.4.373. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  68. Von Wettstein D., Gough S., Kannangara C. G. Chlorophyll Biosynthesis. Plant Cell. 1995 Jul;7(7):1039–1057. doi: 10.1105/tpc.7.7.1039. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  69. Weaver C. D., Shomer N. H., Louis C. F., Roberts D. M. Nodulin 26, a nodule-specific symbiosome membrane protein from soybean, is an ion channel. J Biol Chem. 1994 Jul 8;269(27):17858–17862. [PubMed] [Google Scholar]
  70. Wilson R. C., Long F., Maruoka E. M., Cooper J. B. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell. 1994 Sep;6(9):1265–1275. doi: 10.1105/tpc.6.9.1265. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  71. Wipf L., Cooper D. C. Chromosome Numbers in Nodules and Roots of Red Clover, Common Vetch and Garden Pea. Proc Natl Acad Sci U S A. 1938 Feb;24(2):87–91. doi: 10.1073/pnas.24.2.87. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  72. Yang W. C., Katinakis P., Hendriks P., Smolders A., de Vries F., Spee J., van Kammen A., Bisseling T., Franssen H. Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J. 1993 Apr;3(4):573–585. doi: 10.1046/j.1365-313x.1993.03040573.x. [DOI] [PubMed] [Google Scholar] · DOI
  73. Yang W. C., de Blank C., Meskiene I., Hirt H., Bakker J., van Kammen A., Franssen H., Bisseling T. Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell. 1994 Oct;6(10):1415–1426. doi: 10.1105/tpc.6.10.1415. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  74. de Bruijn F. J., Rossbach S., Schneider M., Ratet P., Messmer S., Szeto W. W., Ausubel F. M., Schell J. Rhizobium meliloti 1021 has three differentially regulated loci involved in glutamine biosynthesis, none of which is essential for symbiotic nitrogen fixation. J Bacteriol. 1989 Mar;171(3):1673–1682. doi: 10.1128/jb.171.3.1673-1682.1989. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  75. de Maagd R. A., Rao A. S., Mulders I. H., Goosen-de Roo L., van Loosdrecht M. C., Wijffelman C. A., Lugtenberg B. J. Isolation and characterization of mutants of Rhizobium leguminosarum bv. viciae 248 with altered lipopolysaccharides: possible role of surface charge or hydrophobicity in bacterial release from the infection thread. J Bacteriol. 1989 Feb;171(2):1143–1150. doi: 10.1128/jb.171.2.1143-1150.1989. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  76. van Spronsen P. C., Bakhuizen R., van Brussel A. A., Kijne J. W. Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol. 1994 Jun;64(1):88–94. [PubMed] [Google Scholar]
  77. van de Wiel C., Scheres B., Franssen H., van Lierop M. J., van Lammeren A., van Kammen A., Bisseling T. The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules. EMBO J. 1990 Jan;9(1):1–7. doi: 10.1002/j.1460-2075.1990.tb08073.x. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

Authors
Mylona, P., Pawlowski, K., & Bisseling, T.
Affiliations
Wageningen University & Research (NL)
ORCID
Venue
The Plant Cell
Publisher
Oxford University Press (OUP)
Published
1995-07-01
Volume
7
Issue
7
Pages
869-885
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
DOI
10.1105/tpc.7.7.869
PMC
PMC160880
OpenAlex
W2124121884
Cited by
692
References
0
Citations by year
2026: 9 · 2025: 16 · 2024: 38 · 2023: 17 · 2022: 17 · 2021: 21 · 2020: 17 · 2019: 24 · 2018: 12 · 2017: 17 · 2016: 10 · 2015: 18 · 2014: 15 · 2013: 18 · 2012: 14
FWCI
58.23
Type
journal article
Language
en
Open access
Licence
aspb.org/publications/aspb-journals/open-articles (vor, 366 d)
Locations
  • The Plant Cell (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Socio-Environmental Systems Modeling (acceptedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Legume Nitrogen Fixing Symbiosis
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Nematode management and characterization studies
Keywords
symbiotic nitrogen fixation, rhizobia, Fabaceae, root nodules, nodulin genes, lipooligosaccharide, rhizobial infection, nodulation, actinorhizal nodules

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review