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Plant Cell. Oct 1996; 8(10): 1885–1898.
PMCID: PMC161322

Rhizobium symbiosis: nod factors in perspective.

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Selected References

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  • Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé JC, 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. [PMC free article] [PubMed]
  • Atkinson EM, Palcic MM, Hindsgaul O, Long SR. 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. [PMC free article] [PubMed]
  • Bauer P, Crespi MD, Szécsi J, Allison LA, Schultze M, Ratet P, Kondorosi E, Kondorosi A. Alfalfa Enod12 genes are differentially regulated during nodule development by Nod factors and Rhizobium invasion. Plant Physiol. 1994 Jun;105(2):585–592. [PMC free article] [PubMed]
  • Bec-Ferté MP, Krishnan HB, Promé D, Savagnac A, Pueppke SG, Promé JC. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257. Biochemistry. 1994 Oct 4;33(39):11782–11788. [PubMed]
  • Bent AF. Plant Disease Resistance Genes: Function Meets Structure. Plant Cell. 1996 Oct;8(10):1757–1771. [PMC free article] [PubMed]
  • Bloemberg GV, Kamst E, Harteveld M, van der Drift KM, Haverkamp J, Thomas-Oates JE, Lugtenberg BJ, Spaink HP. A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors. Mol Microbiol. 1995 Jun;16(6):1123–1136. [PubMed]
  • Bourdineaud JP, Bono JJ, Ranjeva R, Cullimore JV. Enzymatic radiolabelling to a high specific activity of legume lipo-oligosaccharidic nodulation factors from Rhizobium meliloti. Biochem J. 1995 Feb 15;306(Pt 1):259–264. [PMC free article] [PubMed]
  • Brewin NJ. Development of the legume root nodule. Annu Rev Cell Biol. 1991;7:191–226. [PubMed]
  • Caetano-Anollés G, Gresshoff PM. Plant genetic control of nodulation. Annu Rev Microbiol. 1991;45:345–382. [PubMed]
  • Cárdenas L, Domínguez J, Quinto C, López-Lara IM, Lugtenberg BJ, Spaink HP, Rademaker GJ, Haverkamp J, Thomas-Oates JE. Isolation, chemical structures and biological activity of the lipo-chitin oligosaccharide nodulation signals from Rhizobium etli. Plant Mol Biol. 1995 Nov;29(3):453–464. [PubMed]
  • Carlson RW, Price NP, Stacey G. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol Plant Microbe Interact. 1994 Nov-Dec;7(6):684–695. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Cren M, Kondorosi A, Kondorosi E. NolR controls expression of the Rhizobium meliloti nodulation genes involved in the core Nod factor synthesis. Mol Microbiol. 1995 Feb;15(4):733–747. [PubMed]
  • Crespi MD, 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. [PMC free article] [PubMed]
  • Dangl JL, Dietrich RA, Richberg MH. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. [PMC free article] [PubMed]
  • De Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Schiavo FL, Terzi M, Bisseling T, Van Kammen A, et al. Rhizobium Lipooligosaccharides Rescue a Carrot Somatic Embryo Mutant. Plant Cell. 1993 Jun;5(6):615–620. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Dénarié J, Debellé F, Rosenberg C. Signaling and host range variation in nodulation. Annu Rev Microbiol. 1992;46:497–531. [PubMed]
  • Downie JA. Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol. 1994 Sep;2(9):318–324. [PubMed]
  • Downie JA, Surin BP. 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. [PubMed]
  • Ehrhardt DW, Atkinson EM, Long SR. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science. 1992 May 15;256(5059):998–1000. [PubMed]
  • Ehrhardt DW, Atkinson EM, Faull KF, Freedberg DI, Sutherlin DP, Armstrong R, Long SR. In vitro sulfotransferase activity of NodH, a nodulation protein of Rhizobium meliloti required for host-specific nodulation. J Bacteriol. 1995 Nov;177(21):6237–6245. [PMC free article] [PubMed]
  • Fisher RF, Long SR. Rhizobium--plant signal exchange. Nature. 1992 Jun 25;357(6380):655–660. [PubMed]
  • Fisher RF, Long SR. 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. [PubMed]
  • Folch-Mallol JL, Marroqui S, Sousa C, Manyani H, López-Lara IM, van der Drift KM, Haverkamp J, Quinto C, Gil-Serrano A, Thomas-Oates J, et al. Characterization of Rhizobium tropici CIAT899 nodulation factors: the role of nodH and nodPQ genes in their sulfation. Mol Plant Microbe Interact. 1996 Apr;9(3):151–163. [PubMed]
  • Geelen D, Leyman B, Mergaert P, Klarskov K, Van Montagu M, Geremia R, Holsters M. NodS is an S-adenosyl-L-methionine-dependent methyltransferase that methylates chitooligosaccharides deacetylated at the non-reducing end. Mol Microbiol. 1995 Jul;17(2):387–397. [PubMed]
  • Hammond-Kosack KE, Jones JD. Resistance gene-dependent plant defense responses. Plant Cell. 1996 Oct;8(10):1773–1791. [PMC free article] [PubMed]
  • Handelsman J, Stabb EV. Biocontrol of Soilborne Plant Pathogens. Plant Cell. 1996 Oct;8(10):1855–1869. [PMC free article] [PubMed]
  • Hirsch AM, Fang Y. Plant hormones and nodulation: what's the connection? Plant Mol Biol. 1994 Oct;26(1):5–9. [PubMed]
  • Horvath B, Heidstra R, Lados M, Moerman M, Spaink HP, Promé JC, 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. [PubMed]
  • Jabbouri S, Fellay R, Talmont F, Kamalaprija P, Burger U, Relić B, Promé JC, Broughton WJ. Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 nod factors. J Biol Chem. 1995 Sep 29;270(39):22968–22973. [PubMed]
  • Jürgens G, Torres Ruiz RA, Berleth T. Embryonic pattern formation in flowering plants. Annu Rev Genet. 1994;28:351–371. [PubMed]
  • Kamst E, van der Drift KM, Thomas-Oates JE, Lugtenberg BJ, Spaink HP. Mass spectrometric analysis of chitin oligosaccharides produced by Rhizobium NodC protein in Escherichia coli. J Bacteriol. 1995 Nov;177(21):6282–6285. [PMC free article] [PubMed]
  • Kurkdjian AC. Role of the Differentiation of Root Epidermal Cells in Nod Factor (from Rhizobium meliloti)-Induced Root-Hair Depolarization of Medicago sativa. Plant Physiol. 1995 Mar;107(3):783–790. [PMC free article] [PubMed]
  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, 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. [PubMed]
  • Löbler M, Hirsch AM. A gene that encodes a proline-rich nodulin with limited homology to PsENOD12 is expressed in the invasion zone of Rhizobium meliloti-induced alfalfa root nodules. Plant Physiol. 1993 Sep;103(1):21–30. [PMC free article] [PubMed]
  • López-Lara IM, van den Berg JD, Thomas-Oates JE, Glushka J, Lugtenberg BJ, Spaink HP. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol. 1995 Feb;15(4):627–638. [PubMed]
  • Mergaert P, Van Montagu M, Promé JC, 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. [PMC free article] [PubMed]
  • Mergaert P, D'Haeze W, Geelen D, Promé D, Van Montagu M, Geremia R, Promé JC, Holsters M. Biosynthesis of Azorhizobium caulinodans Nod factors. Study of the activity of the NodABCS proteins by expression of the genes in Escherichia coli. J Biol Chem. 1995 Dec 8;270(49):29217–29223. [PubMed]
  • Philip-Hollingsworth S, Orgambide GG, Bradford JJ, Smith DK, Hollingsworth RI, Dazzo FB. Mutation or increased copy number of nodE has no effect on the spectrum of chitolipooligosaccharide nod factors made by Rhizobium leguminosarum bv. trifolii. J Biol Chem. 1995 Sep 8;270(36):20968–20977. [PubMed]
  • Poupot R, Martinez-Romero E, Promé JC. 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. [PubMed]
  • Price NP, Carlson RW. Rhizobial lipo-oligosaccharide nodulation factors: multidimensional chromatographic analysis of symbiotic signals involved in the development of legume root nodules. Glycobiology. 1995 Mar;5(2):233–242. [PubMed]
  • Price NP, Relić B, Talmont F, Lewin A, Promé D, Pueppke SG, Maillet F, Dénarié J, Promé JC, Broughton WJ. 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. [PubMed]
  • Rivilla R, Sutton JM, Downie JA. Rhizobium leguminosarum NodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF. Gene. 1995 Aug 8;161(1):27–31. [PubMed]
  • Röhrig H, Schmidt J, Walden R, Czaja I, Miklascaroneviccarons E, Wieneke U, Schell J, John M. Growth of tobacco protoplasts stimulated by synthetic lipo-chitooligosaccharides. Science. 1995 Aug 11;269(5225):841–843. [PubMed]
  • Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, 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. [PMC free article] [PubMed]
  • Schlaman HR, Okker RJ, Lugtenberg BJ. Regulation of nodulation gene expression by NodD in rhizobia. J Bacteriol. 1992 Aug;174(16):5177–5182. [PMC free article] [PubMed]
  • Schultze M, Staehelin C, Röhrig H, John M, Schmidt J, Kondorosi E, Schell J, Kondorosi A. In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2706–2709. [PMC free article] [PubMed]
  • Smit G, de Koster CC, Schripsema J, Spaink HP, van Brussel AA, Kijne JW. Uridine, a cell division factor in pea roots. Plant Mol Biol. 1995 Nov;29(4):869–873. [PubMed]
  • Spaink HP, Lugtenberg BJ. Role of rhizobial lipo-chitin oligosaccharide signal molecules in root nodule organogenesis. Plant Mol Biol. 1994 Dec;26(5):1413–1422. [PubMed]
  • Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJ. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature. 1991 Nov 14;354(6349):125–130. [PubMed]
  • Stacey G, Luka S, Sanjuan J, Banfalvi Z, Nieuwkoop AJ, Chun JY, Forsberg LS, 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. [PMC free article] [PubMed]
  • Staehelin C, Schultze M, Kondorosi E, Kondorosi A. Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa. Plant Physiol. 1995 Aug;108(4):1607–1614. [PMC free article] [PubMed]
  • Stokkermans TJ, Peters NK. Bradyrhizobium elkanii lipo-oligosaccharide signals induce complete nodule structures on Glycine soja Siebold et Zucc. Planta. 1994;193(3):413–420. [PubMed]
  • Stokkermans TJ, Ikeshita S, Cohn J, Carlson RW, Stacey G, Ogawa T, Peters NK. Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja. Plant Physiol. 1995 Aug;108(4):1587–1595. [PMC free article] [PubMed]
  • Sutton JM, Lea EJ, Downie JA. 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. [PMC free article] [PubMed]
  • van Brussel AA, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJ, Kijne JW. 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. [PubMed]
  • van de Sande K, Pawlowski K, Czaja I, Wieneke U, Schell J, Schmidt J, Walden R, Matvienko M, Wellink J, van Kammen A, et al. Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume. Science. 1996 Jul 19;273(5273):370–373. [PubMed]
  • van Eijsden R, Díaz CL, de Pater BS, Kijne JW. Sugar-binding activity of pea (Pisum sativum) lectin is essential for heterologous infection of transgenic white clover hairy roots by Rhizobium leguminosarum biovar viciae. Plant Mol Biol. 1995 Nov;29(3):431–439. [PubMed]
  • van Spronsen PC, Bakhuizen R, van Brussel AA, Kijne JW. 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]
  • van Spronsen PC, van Brussel AA, Kijne JW. Nod factors produced by Rhizobium leguminosarum biovar viciae induce ethylene-related changes in root cortical cells of Vicia sativa ssp. nigra. Eur J Cell Biol. 1995 Dec;68(4):463–469. [PubMed]
  • Wilson RC, Long F, Maruoka EM, Cooper JB. A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells. Plant Cell. 1994 Sep;6(9):1265–1275. [PMC free article] [PubMed]
  • Yang WC, 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. [PMC free article] [PubMed]

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