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Influence ofRhizobium leguminosarum biovartrifolii host specific nodulation genes on the ontogeny of clover nodulation

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Summary

The infection of white clover seedlings byRhizobium strains with different host range properties was assessed using various microscopic techniques. Several wild-type andRhizobium leguminosarum biovarvicias hybrid strains containing definedR. l. bv.trifolii host range genes were used. The morphological changes in the root tissue of uninoculated and rhizobia inoculated white clovers were identified and compared. In particular, changes were observed in the induction of inner cortical cell division, alterations to nodule development and lateral root formation. The responses of the infected roots and the types of structures formed support the hypothesis that lateral roots and nodules may be physiologically homologous structures. To establish a normal pattern of nodulation on white clover roots, both sets of known host specific nodulation genes (operonsnod FERL andnod MNX) ofR. l. bv.trifolii were required. However, some nodule development occurred when only thenod FERL genes were present in the hybrid strain.

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References

  • Canter Cremers HCJ, Spaink HP, Wijfjes AHM, Pees E, Wijffelman CA, Okker RJH, Lugtenberg BJJ (1989) Additional nodulation genes on the Sym plasmid ofRhizobium leguminosarum biovarvicias. Plant Mol Biol 13: 163–174

    PubMed  Google Scholar 

  • Djordjevic MA, Schofield PR, Ridge RW, Morrison NA, Bassam BJ, Plazinski J, Watson JM, Rolfe BG (1985)Rhizobium nodulation genes involved in root hair curling (Hac) are functionally conserved. Plant Mol Biol 4: 147–160

    Google Scholar 

  • —, Innes RW, Wijffelman CA, Schofield PR, Rolfe BG (1986) Nodulation of specific legumes is controlled by several loci inRhizobium trifolii. Plant Mol Biol 6: 389–403

    Google Scholar 

  • —, Redmond JW, Batley M, Rolfe BG (1987) Clovers secrete specific phenolic compounds which either stimulate or repressnod gene expression inRhizobium trifolii. EMBO J 6: 1173–1179

    Google Scholar 

  • Downie JA (1989) ThenodL gene fromRhizobium leguminosarum is homologous to the acetyl transferases encoded bylacA andcysE. Mol Microbiol 3: 1649–1651

    PubMed  Google Scholar 

  • —, Marie C, Scheu AK, Firmin JL, Wilson KE, Davies AE, Cubo TM, Mavridou A, Johnston AWB, Economou A (1991) Genetic and biochemical studies on the nodulation genes ofRhizobium leguminosarum bv.viciae. In: Hennecke H, Verma DPS (eds) Advances in molecular genetics of plant-microbe interactions. Kluwer, Dordrecht, pp 134–141

    Google Scholar 

  • Gresshoff PM, Delves AC (1986) Plant genetic approaches to symbiotic nodulation and nitrogen fixation in legumes. In: Blonstein AD, King PJ (eds) A genetic approach to plant biochemistry. Springer, Wien New York, pp 159–206 [Dennis ES et al (eds) Plant gene research]

    Google Scholar 

  • Hirsch AM, Drake D, Jacobs TW, Long SR (1985) Nodules are induced on alfalfa roots byAgrobacterium tumefaciens andRhizobium trifolii containing small segments of theRhizobium meliloti nodulation region. J Bacteriol 161: 223–230

    PubMed  Google Scholar 

  • Hrabak EM, Truchet GL, Dazzo FB, Covers F (1985) Characterization of the anomalous infection and nodulation of subterranean clover roots byRhizobium leguminosarum 1020. J Gen Microbiol 131: 3287–3302

    Google Scholar 

  • Huang SZ, Djordjevic MA, Rolfe BG (1988) Characterisation of aberrant infection events induced onTrifolium subterraneum byRhizobium trifolii region II mutants. J Plant Physiol 133: 16–24

    Google Scholar 

  • — — — (1993) Microscopic analysis of the effect ofRhizobium leguminosarum biovartrifolii host specific nodulation genes in the infection of white clovers. Protoplasma 172: 180–190

    Google Scholar 

  • Johnston AWB, Beringer JE (1975) Identification of theRhizobium strains in pea root nodules using genetic markers. J Gen Microbiol 87: 343–350

    Google Scholar 

  • Lerouge P, Roche Ph, Faucher C, Mallet F, Truchet G, Prome JC, Denarie J (1990) Symbiotic host-specificity ofRhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781–784

    Google Scholar 

  • Lewis-Henderson WR, Djordjevic MA (1991)nodT, a positivelyacting, cultivar controlling nodulation ofTrifolium subterraneum byRhizobium leguminosarum biovartrifolii. Plant Mol Biol 16: 515–526

    PubMed  Google Scholar 

  • Libbenga KR, Bogers RJ (1974) Root-nodule morphogenesis. In: Quispel A (ed) The biology of nitrogen fixation. North-Holland, Amsterdam, pp 430–472

    Google Scholar 

  • —, Harkes PAA (1973) Initial proliferation of cortical cells in the formation of root nodules inPisum sativum L. Planta 114: 17–28

    Google Scholar 

  • Long SR (1989)Rhizobium-legame nodulation: life together in the underground. Cell 56: 203–214

    PubMed  Google Scholar 

  • McIver J, Djordjevic MA, Weinman JJ, Bender GL, Rolfe BG (1989) Extension of host range ofRhizobium leguminosarum bv.trifolii caused by point mutations innodD that result in alterations in regulatory function and recognition of inducer molecules. Mol Plant Microbe Interact 2: 97–106

    PubMed  Google Scholar 

  • Nap J-P, Bisseling T (1990) Developmental biology of a plant-prokaryote symbiosis: the legume root nodule. Science 250: 948–954

    Google Scholar 

  • Nutman PS (1948) Physiological studies on nodule formation. I. The relation between nodulation and lateral root formation in red clover. Ann Bot 12: 81–94

    Google Scholar 

  • — (1949) Physiological studies on nodule formation. II. The influence of delayed inoculation on the rate of nodulation in red clover. Ann Bot 13: 261–283

    Google Scholar 

  • — (1952) Studies on the physiology of nodule formation. III. Experiments on the excision of root-tips and nodules. Ann Bot 16: 79–102

    Google Scholar 

  • Phillips DA (1971) Abscisic acid inhibition of root nodule initiation onPisum sativum. Planta 100: 181–190

    Google Scholar 

  • Rolfe BG, Gresshoff PM (1988) Genetic analysis of legume nodule initiation. Annu Rev Plant Physiol Plant Mol Biol 39: 297–319

    Google Scholar 

  • — —, Shine J, Vincent JM (1980) Interaction between a non-nodulating and an ineffective mutant ofRhizobium trifolii resulting in effective (nitrogen-fixing) nodulation. Appl Environ Microbiol 39: 449–452

    Google Scholar 

  • —, Weinman JJ, Djordjevic MA (1989 a) Host specificity inRhizobium. In: Kosuge T, Nester EW (eds) Plant-microbe interactions: molecular and genetic perspectives, vol 3. McGraw-Hill, New York, pp 421–456

    Google Scholar 

  • —, Sargent CL, Weinman JJ, Djordjevic MA, Mclver J, Redmond JW, Batley M, Yuan DC, Sutherland MW (1989 b) Signal exchange betweenR. trifolii and clovers. In: Lugtenberg BJJ (ed) Signal molecules in plants and plant-microbe interactions. Springer, Berlin Heidelberg New York Tokyo, pp 303–310 (NATO ASI Series, series H, vol 36)

    Google Scholar 

  • Rudall P (1987) Anatomy of flowering plants. An introduction to structure and development. Edward Arnold, Sevenoaks, Kent Salisbury FB, Ross CW (1985) Plant physiology, 2nd edn. Wadsworth, Belmont, CA

    Google Scholar 

  • Schuch W, Knight M, Bird A, Grima-Pettenati J (1990) Modulation of plant gene expression. In: Lycett GW, Grierson D (eds) Genetic engineering of crop plants. Butterworths, London, pp 221–230

    Google Scholar 

  • Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka JN, Endre G, Gero SD, Kondorosi A (1992)Rhizobium meliloti produces a family of sulfated lipo-oligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89: 192–916

    PubMed  Google Scholar 

  • Spaink HP, Wijffelman CA, Pees E, Okker RJH, Lugtenberg BJJ (1987)Rhizobium nodulation genenodD as a determinant of host specificity. Nature 328: 337–340

    Google Scholar 

  • —, Sheeley DM, van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity ofRhizobium. Nature 354: 125–130

    PubMed  Google Scholar 

  • —, Aarts A, Stacey G, Bloemberg GV, Lugtenberg BJJ, Kennedy EP (1992) Detection and separation ofRhizobium andBradyrhizobium Nod metabolites using thin-layer chromatography. Mol Plant Microbe Interact 5: 72–80

    PubMed  Google Scholar 

  • Sleeves TA, Sussex IM (1989) Patterns in plant development. Cambridge University Press, Cambridge

    Google Scholar 

  • Surin BP, Downie JA (1989)Rhizobium leguminosarum genes required for expression and transfer of host specific nodulation. Plant Mol Biol 12: 19–29

    Google Scholar 

  • Truchet G, Debelle F, Vasse J, Terzaghi B, Garnerone A-M, Rosenberg C, Batut J, Maillet F, Denarie J (1985) Identification of aRhizobium meliloti pSym 2011 region controlling the host specificity of root hair curling and nodulation. J Bacteriol 164: 1200–1210

    PubMed  Google Scholar 

  • —, Camut S, de Billy F, Odorico R, Vasse J (1989) TheRhizobiumlegume symbiosis two methods to discriminate between nodules and other root-derived structures. Protoplasma 149: 82–88

    Google Scholar 

  • Van Brussel AAN, Recourt K, Pees E, Spaink HP, Tak T, Wijffelman CA, Kijne JW, Lugtenberg BJJ (1990) A biovar-specific signal ofRhizobium leguminosarum bv.viciae induces increased nodulation gene-inducing activity in root exudate ofVicia sativa subsp.nigra. J Bacteriol 172: 5394–5401

    PubMed  Google Scholar 

  • Weinman JJ, Djordjevic MA, Sargent CL, Dazzo FB, Rolfe BG (1988) A molecular analysis of the host range genes ofRhizobium trifolii. In: Palacios R, Verma DPS (eds) Molecular genetics of plant-microbe interactions. American Phytopathological Society, St. Paul, MN, pp 33–34

    Google Scholar 

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Mclver, J., Djordjevic, M.A., Weinman, J.J. et al. Influence ofRhizobium leguminosarum biovartrifolii host specific nodulation genes on the ontogeny of clover nodulation. Protoplasma 172, 166–179 (1993). https://doi.org/10.1007/BF01379374

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