Abstract
Root exudate of Vicia sativa contains 7 inducers for the nodA promoter of Rhizobium leguminosarum biovar viciae. Six of these inducers are flavanones. One inducer was identified as 3,5,7,3′-tetrahydroxy-4′-methoxyflavanone, and a second inducer most likely is 7,3′-dihydroxy-4′-methoxyflavanone. The inducing activity of these compounds and the other inducers depends on the nodD gene present in the test strains, which orginated either from R. leguminosarum biovars viciae or trifolii, or from R. meliloti. Three inducers are ‘common’, three others almost exclusively induce the nodA promoter in the presence of the R. leguminosarum biovar viciae nodD gene, and the last one is active with the noD genes of either R. leguminosarum biovar viciae or that of R. meliloti. Testing of a large number of flavonoids revealed two classes of structural features required for inducing ability: (i) features required for induction in general, and (ii), features restricting the inducing ability to (a) specific nodD gene(s). These features are discussed in relation to current models of the process of nodD-mediated transcription activation of the inducible nod genes.
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References
Bender GL, Nayudu M, LeStrange KK, Rolfe BG: The nodD1 gene of Rhizobium strain NGR234 is a key determinant in the extension of host range to the nonlegume Parasponia. MPMI 1: 259–266 (1988).
Burn J, Rossen L, Johnston AWB: Four classes of mutations in the nodD gene of Rhizobium leguminosarum biovar, viciae that affect its ability to autoregulate and/or activate other nod genes in the presence of flavonoids inducers. Genes and Development 1: 456–464 (1987).
Canter-Cremers HCJ, VanBrussel AAN, Plazinski J, Rolfe BG: Sym plasmid and chromosomal gene products of Rhizobium trifolii elicit developmental responses on various legume roots. J Plant Physiol 122: 25–40 (1986).
Djordjevic MA, McIver J, Bender GL, Weinman JJ, Rolfe BG: Point mutations in nodD alters function and confers extension of host range of Rhizobium leguminosarum biovar trifolii to Parasponia. In: Palacios R, Verma DPS (eds) Molecular Genetics of Plant-Microbe Interactions 1988, pp. 101–102. APS Press, St Paul, MN (1988).
Faucher C, Maillet F, Vasse J, Rosenberg C, VanBrussel AAN, Truchet G, Dénarié J: Evidence that Rhizobium meliloti nodH gene determines host specificity via an extracellular signal. J Bact 170: 5489–5499 (1988).
Firmin JL, Wilson KE, Rossen L, Johnston AWB: Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature (London) 324: 90–92 (1986).
Fisher RF, Egelhoff T, Mulligan JT, Long SR: Specific biding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes and Devel 2: 282–293 (1988).
Hong GF, Burn JE, Johnston AWB: Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucl Acids Res 15: 9677–9690 (1987).
Honma MA, Ausubel F: Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory protein. Proc Natl Acad Sci USA 84: 8558–8562 (1987).
Horvath B, Bachem CW, 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 6: 841–848 (1987).
Hostettman K, Hostetteman M: Isolation techniques for flavonoids. In: Harborne JB, Marbry TJ (eds) The Flavonoids, Advances in the Research, pp. 1–18. Chapman and Hall, London New York (1982).
Innes RW, Kuempel PL, Plazinski J, Canter Cremers HCJ, Rolfe BG, Djordjevic MA: Plant factors induce expression of nodulation and host-range genes in R. trifolii. Mol Gen Genet 201: 426–432 (1985).
Jurd L: Spectral properties of flavonoid compounds. In: Geissman TA (ed) The Chemistry of Flavonoid Compounds, pp. 107–155, MacMillan, New York (1962).
Kondorosi A, Kondorosi E, Györgypal Z, Banfalvi Z, Gyuris J, Putnoky P, Grosskopf E, John M, Schmidt J, Cam Ha DT, Lados M, Slaska-Kiss K, Schell J: Rhizobium meliloti nod and fix genes controlling the initiation and development of root nodules. In: Bothe H, DeBruijn FJ, Newton WE (eds) Nitrogen fixation: Hundred Years After, pp. 399–403. Gustav Fisher, Stuttgart, New York (1988).
Kosslak RM, Bookland R, Barkei J, Paaren HE, Applebaum ER: Induction of Bradyhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci USA 84: 7428–7432 (1987).
Lugtenberg BJJ, VanBrussel AAN, Okker RJH, Recourt K, Schlaman HRM, Spaink HP, Wijffelman CA, Zaat SAJ: Mechanism of activation of Rhizobium nodD gene. In: Palacios R, Verma DPS (eds) Molecular Genetics of Plant-Microbe Interaction 1988, pp 79–83. APS Press, St Paul, MN (1988).
Mabry TJ, Markham KR, Thomas MB: The Systematic Identification of Flavonoids. Springer-Verlag, Berlin/Heidelberg/New York (1970).
Miller JH: Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1972).
Mulligan JT, Long SR: Induction of Rhizobium meliloti nodC expression by plant root exudate requires nodD. Proc Natl Acad Sci USA 82: 6609–6613 (1985).
Peters NK, Frost JW, Long SR: A plant flavone, luteolin, induces expression of Rhizobium meliloti genes. Science 233: 977–980 (1986).
Recourt K, VanBrussel A, Driessen A, Lugtenberg B: The uptake of the nod gene inducer naringenin by Rhizobium leguminosarum. In: Bothe H, DeBruijn FJ, Newton WE (eds) Nitrogen Fixation: Hundred Years After, p. 467. Gustav Fischer, Stuttgart/New York (1988).
Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG: Elavones induce expression of nodulation genes in Rhizobium. Nature (London) 323: 632–635 (1986).
Rolfe BG: Flavones and isoflavones as inducing substances of legume nodulation. BioFactors 1: 3–10 (1988).
Rossen L, Shearman CA, Johnston AWB, Downie JA: The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodA,B,C genes. EMBO J 4: 3369–3373 (1985).
Sadowsky MJ, Olson ER, Foster VE, Kosslak RM, Verma DP: Two host-inducible genes of Rhizobium fredii and characterization of the inducing compound. J Bact 170: 171–178 (1988).
Shearman CA, Rossen L, Johnston AWB, Downie JA: 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 5: 647–652 (1986).
Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ: Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9: 27–39 (1987).
Spaink HP, Wijffelman CA, Pees E, Okker RJH, Lugtenberg BJJ: Rhizobium nodulation gene nodD as a determinant of host specificity. Nature (London) 328: 337–340 (1987).
Spaink H, Okker R, Wijffelman C, Lugtenberg B: Fine mapping of the Rhizobium nodD gene. In: Palacios R, Verma DPS (eds) Molecular genetics of Plant-Microbe interactions 1988, pp. 90–91. APS Press, St Paul, MN (1988).
VanBrussel AAN, Zaat SAJ, Canter Cremers HCJ, Wijffelman CA, Pees E, Tak T, Lugtenberg BJJ: 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 Bact 165: 517–522 (1986).
VandeCasteele K, Geiger H, VanSumere CF: Sepa ration of flavonoids by reversed-phase high-performance liquid chromatography. J Chromatog 240: 81–94 (1982).
Vincent JM: Factors controlling the legume-Rhizobium symbiosis. In: Newton WE, Orme-Johnson (eds) Nitrogen Fixation, pp. 103–129. University Park Press, Baltimore (1980).
Wijffelman CA, Zaat B, Spaink H, Mulders I, VanBrussel AAN, Brussel AAN, Okker R, DeMaagd R, Lugtenberg BJJ: Induction of Rhizobium nod genes by flavonoids: differential adaptation of promoter, nodD gene and inducers for various cross-inoculation groups. In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic and Pathogenic Interactions, NATO ASI Series, Vol H4, pp. 123–135. Springer-Verlag, Berlin/Heidelberg (1986).
Zaat SAJ, Wijffelman CA, Spaink HP, VanBrussel AAN, Okker RJH, Lugtenberg BJJ: Induction of the nodA promoter of Rhizobium leguminosarum Sym plasmid pRL1JI by plant flavanones and flavones. J Bact 169: 198–204 (1987).
Zaat SAJ, Wijffelman CA, Mulders IHM, VanBrussel AAN, Lugtenberg BJJ: Root exudates of various host plants of Rhizobium leguminosarum contain different sets of inducers of Rhizobium nodulation genes. Plant Physiol 86: 1298–1303 (1988).
Zaat SAJ, Spaink HP, Wijffelman CA, VanBrussel AAN, Okker RJH, Lugtenberg BJJ: Flavonoid compounds as molecular signals in Rhizobium-legume symbiosis. In: Scannerini S (ed) Cell to Cell Signals in Plant, Animal and Microbial Symbiosis. NATO ASI Series, vol. H17, pp. 189–205. Springer-Verlag, Berlin/Heidelberg (1988).
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Zaat, S.A.J., Schripsema, J., Wijffelman, C.A. et al. Analysis of the major inducers of the Rhizobium nodA promoter from Vicia sativa root exudate and their activity with different nodD genes. Plant Mol Biol 13, 175–188 (1989). https://doi.org/10.1007/BF00016136
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DOI: https://doi.org/10.1007/BF00016136