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Plant gene expression during effective and ineffective nodule development of the tropical stem-nodulated legume Sesbania rostrata

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Abstract

The expression of plant genes during symbiosis of Sesbania rostrata with Rhizobium sp. and Azorhizobium caulinodans was studied by comparing two-dimensional PAGE patterns of in vitro translation products of poly(A)+ RNA from uninfected roots and stems with that of root and stem nodules. Both types of nodules are essentially similar, particularly when stem nodules are formed in the dark. We detected the specific expression of at least 16 genes in stem and root nodules and observed the stimulated expression of about 10 other genes in both nodules. Six of the nodule-specific translation products (apparent molecular masses around 16 kDa) cross-react with an antiserum raised against leghemoglobin purified from Sesbania rostrata stem nodules. During stem nodule development, most of the nodule-stimulated genes are expressed concomitantly with leghemoglobin at day 12 after inoculation. However, some genes are already stimulated at days 6–7, some others later in development (day 18), and some are transiently activated. Patterns of root nodules induced by either Azorhizobium caulinodans strain ORS571, capable of effective root and stem nodulation, or Rhizobium sp. strain ORS51, capable of effective root nodulation only, are very similar except for a specific 37.5 kDa polypeptide. Several types of ineffective stem and root nodules were studied; in every case the amount of leghemoglobin components appeared reduced together with most of the nodule-stimulated polypeptides.

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References

  1. Alazard D: Stem and root nodulation in Aeschynomene spp. Appl Environ Microbiol 50(3): 732–734 (1985).

    Google Scholar 

  2. Appleby C: Leghemoglobin and Rhizobium respiration. In: Briggs WR (ed.) Ann Rev Plant Physiol 35: 443–478 (1984).

  3. Appleby CA, Bergersen FJ: Preparation and experimental use of leghemoglobin. In: Bergersen FJ (ed.) Methods for Evaluating Biological Nitrogen Fixation. John Wiley, London.

  4. Bergmann H, Preddie E, Verma DPS: Nodulin 35: a subunit of specific uricase (uricase II) induced and localized in the uninfected cells of soybean nodules. EMBO J 2(12): 2333–2339 (1983).

    Google Scholar 

  5. Bisseling T, Been C, Klugkist J, VanKammen A, Nadler K: Nodule-specific host proteins in effective and ineffective root nodules of Pisum sativum. EMBO J 2: 961–966 (1983).

    Google Scholar 

  6. Bogusz D, Kortt AA, Appleby CA: Sesbania rostrata root and stem nodule leghemoglobin: purification and relationships amongst the seven major components. Arch Biochem Biophys 254(1): 263–271 (1987).

    Google Scholar 

  7. Cullimore JV, Lara M, Lea PJ, Miflin BJ: Purification and properties of two forms of glutamine synthetase from the plant fraction of Phaseolus root nodules. Planta 157: 245–253 (1983).

    Google Scholar 

  8. DeLajudie P, Huguet T: Plant gene expression during effective and ineffective nodule development of the tropical stemnodulated legume Sesbania rostrata. In: Verma DPS, Brisson N (Eds.) Molecular Genetics of Plant-Microbe Interactions. Martinus Nijhoff, Dordrecht (1987) pp. 130–132.

    Google Scholar 

  9. Denèfle P, Kush A, NOrel F, Paquelin A, Elmerich C: Biochemical and genetic analysis of the nif HDKE of Rhizobium ORS571. Mol Gen Genet 207: 280–287 (1987).

    Google Scholar 

  10. Donald RGK, Nees DW, Raymond CK, Loroch AI, Ludwig RA: Characterization of three genomic loci encoding Rhizobium sp. strain ORS571 N2 fixation genes. J Bact 165(1): 72–81 (1986).

    Google Scholar 

  11. Dreyfus BL, Dommergues YR: Nitrogen fixing nodules induced by Rhizobium on the stem of the tropical legume Sesbania rostrata. FEMS Microbiol Lett 10: 313–317 (1981).

    Google Scholar 

  12. Dreyfus BL, Elmerich C, Dommergues YR: Free-living Rhizobium strain able to grow under N2 as the sole nitrogen source. Appl Envir Microbiol 45: 711 (1983).

    Google Scholar 

  13. Dreyfus BL, Garcia JL, Gillys M: Characterization of Azorhizobium caulinodans gen. nov., sp. nov, a stemnodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bact, In press (1987).

  14. Dreyfus BL, Rinaudo G, Dommergues YR: Observations on the use of Sesbania rostrata as green manure in paddy fields. MIRCEN J 1: 111–121 (1985).

    Google Scholar 

  15. Duhoux E, Dreyfus BL: Nature des sites d'infection par le Rhizobium de la tige de la légumineuse Sesbania rostrata Brem CR Acad Sci 294: 407–411 (1982).

    Google Scholar 

  16. Duhoux E: Ontogénèse des nodules caulinaires de Sesbania rostrata (légumineuse) Can J Bot 62: 982–994 (1984).

    Google Scholar 

  17. Elmerich C, Dreyfus BL, Reysset G, Aubert JP: Genetic analysis of nitrogen fixation in a tropical fast-growing Rhizobium. EMBO J 1(4): 499–503 (1982).

    Google Scholar 

  18. Fortin MG, Morrison NA, Verma DPS: Nodulin 26, a peribacteroid membrane nodulin is expressed independantly of the development of the peribacteroid compartment. Nucl Acids Res 15(2): 813–824 (1987).

    Google Scholar 

  19. Fuchsman WH, Appleby CA: Separation and determination of relative concentrations of the homogenous components of soybean leghemoglobins by isoelectric focusing. Biochim Biophys Acta 579: 314–324 (1979).

    Google Scholar 

  20. Fuller F, Künstner PW, Nguyen T, Verma DPS: Soybean nodulin genes: analysis of cDNA clones reveals several major tissue-specific sequences in nitrogen-fixing root nodules. Proc Natl Acad Sci USA 80: 2594–2598 (1983).

    Google Scholar 

  21. Fuller F, Verma DPS: Appearance and accumulation of nodulin mRNAs and their relationship to the effectiveness of root nodules. Plant Mol Biol 3: 21–28 (1984).

    Google Scholar 

  22. Gebhardt C, Oliver JE, Forde BG, Saarelainen R, Miflin BJ: Primary structure and differential expression of glutamine synthetase genes in nodules, roots and leaves of Phaseolus vulgaris. EMBO J 5(7): 1429–1435 (1986).

    Google Scholar 

  23. Gloudemans T, deVries S, Bussink HJ, Malik NSA, Franssen HJ, Louwerse J, Bisseling T: Nodulin gene expression during soybean (Glycine max) nodule development. Plant Mol Biol 8: 395–403 (1987).

    Google Scholar 

  24. Govers F, Gloudemans T, Moerman M, VanKammen A, Bisseling T: Expression of plant genes during the development of pea root nodules. EMBO J 4(4): 861–867 (1985).

    Google Scholar 

  25. Hardy RWF, Holsten RD, Jackson EK, Burns RC: The acetylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43: 1185–1207 (1968).

    Google Scholar 

  26. Jacobs FA, Zhang M, Fortin MG, Verma DPS: Several nodulins of soybean share structural domains but differ in their subcellular locations. Nucl Acids Res 15(3): 1271–1280 (1987).

    Google Scholar 

  27. Katinakis P, Verma DPS: Nodulin-24 gene of soybean codes for a peptide of the peribacteroid membrane and was generated by tandem duplication of a sequence resembling an insertion element. Proc Natl Acad Sci USA 82: 4157–4161 (1985).

    Google Scholar 

  28. Kush A, Elmerich C, Aubert JP: Nitrogenase of Sesbania Rhizobium strain ORS571: purification properties, and “Switch-off” by ammonia. J Gen Microbiol 131: 1765–1777 (1985).

    Google Scholar 

  29. Lang-Unnasch N, Ausubel FM: Nodule-specific polypeptides from effective alfalfa root nodules and from ineffective nodules lacking nitrogenase. Plant Physiol 77: 833–839 (1985).

    Google Scholar 

  30. Laskey RA, Mills AD: Quantitative film detection of 3-H and 14-C in polyacrylamide gels by fluorography. Eur J Biochem 56: 335–341 (1975).

    Google Scholar 

  31. Legocki RP, Verma DPS: Identification of “Nodulespecific” host proteins (nodulins) involved in the development of Rhizobium-legume symbiosis. Cell 20: 153–163 (1980).

    Google Scholar 

  32. Ludwig RA: Rhizobium sp. ORS571 grows synergistically on N2 and nicotinate as N sources. J Bact 165(I): 304–307 (1986).

    Google Scholar 

  33. Lullien V, Barker DG, deLajudie P, Huguet T: Plant gene expresion in effective and ineffective root nodules of alfalfa (Medicago sativa). Plant Mol Biol 9: 469–478 (1987).

    Google Scholar 

  34. Nguyen T, Zelechowska M, Foster V, Bergmann H, Verma DPS: Primary structure of the soybean nodulin 35 gene encoding uricase II localized in the peroxysomes of uninfected cells of nodules. Proc Natl Acad Sci USA 82: 5040–5044 (1985).

    Google Scholar 

  35. Norel F, Elmerich C: Nucleotide sequence and functional analysis of the two nif H copies of Rhizobium ORS571. J Gen Microbiol 133: 1563–1576 (1987).

    Google Scholar 

  36. O'Farrell PH: High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250(10): 4007–4021 (1975).

    Google Scholar 

  37. Olsson JE, Rolfe BG: Stem and root nodulation of the tropical legume Sesbania rostrata by Rhizobium strains ORS571 and WE7. J Plant Physiol 121: 199–210 (1985).

    Google Scholar 

  38. Pawlowski K, Ratet P, Schell J, deBruijn FJ: Cloning and characterization of nifA and ntrC genes of the stemnodulating bacterium ORS571, the nitrogen-fixing symbiont of Sesbania rostrata: regulation of nitrogen fixation (nif) genes in the free-living versus symbiotic state. Mol Gen Genet 206: 207–219 (1987).

    Google Scholar 

  39. Rinaudo G, Moudiongui A: Fixation d'azote par Sesbania rostrata: son utilisation comme engrais vert. Bull Rech Agron Gembloux 20(3/4): 833–849 (1985).

    Google Scholar 

  40. Robertson JG, Wells B, Bisseling T, Famden KJF, Johnston AWB: Immuno-gold localization of leghaemoglobin in cytoplasm in nitrogen-fixing root nodules of pea. Nature 311: 254–257 (1984).

    Google Scholar 

  41. Rochaix JD, Malnoe PM: Use of DNA-RNA hybridization for locating chloroplast genes and for estimating the size and abundance of chloroplast DNA transcripts. In: Edelman et al. (eds.) Methods in Chloroplast Molecular Biology, Elsevier Biomedical Press, Amsterdam, pp. 477–490 (1982).

    Google Scholar 

  42. Schaede R: Die Knöllchen der adventiven wasserwurzeln von Neptunia oleracea und ihre Bakteriensymbiose. Planta 31: 1–21 (1940).

    Google Scholar 

  43. Sengupta-Gopalan C, Pitas JW: Expression of nodulespecific glutamine synthetase genes during nodule development in soybeans. Plant Mol Biol 7: 189–199 (1986).

    Google Scholar 

  44. Tsien HC, Dreyfus BL, Schmidt EL: Initial stage in the morphogenesis of nitrogen-fixing stem nodules of Sesbania rostrata. J Bact 119: 986–999 (1983).

    Google Scholar 

  45. Van denEede G, Dreyfus BL, Goethals K, VanMontagu M, Holsters M: Identification and cloning of nodulation genes from the stem-nodulating bacterium ORS571. Mol Gen Genet 206: 291–299 (1987).

    Google Scholar 

  46. VanKammen A: Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol Biol Rep 2(2): 43–45 (1984).

    Google Scholar 

  47. Verma DPS, Bal AK: Intracellular site of synthesis and localization of leghemoglobin in root nodules. Proc Natl Acad Sci USA 73(11): 3843–3847 (1976).

    Google Scholar 

  48. Verma DPS, Fortin MG, Stanley J, Mauro VP, Purohit S, Morrisen N: Nodulins and nodulin genes in Glycine max. Plant Mol Biol 7: 51–61 (1986).

    Google Scholar 

  49. Vincent JM: A manual for practical study of root nodule bacteria. International Biological Programme Handbook M15. Blackwell Scientific Publications, Oxford.

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  1. Philippe de Lajudie

    Present address: Laboratoire de Biologie des Sols, ORSTOM, B.P. 1386, Dakar, Sénégal

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  1. Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes INRA-CNRS, BP 27, Auzeville, 31326, Castanet-Tolosan Cedex, France

    Philippe de Lajudie & Thierry Huguet

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  1. Philippe de Lajudie
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  2. Thierry Huguet
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de Lajudie, P., Huguet, T. Plant gene expression during effective and ineffective nodule development of the tropical stem-nodulated legume Sesbania rostrata . Plant Mol Biol 10, 537–548 (1988). https://doi.org/10.1007/BF00033608

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  • DOI: https://doi.org/10.1007/BF00033608

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