Skip to main content
Log in

The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENOD3/14 and is expressed after the leghaemoglobin genes

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The pea late nodulin gene PsNOD6 has been cloned and sequenced. PsNOD6 is homologous to the pea early nodulin genes PsNOD3 and PsENOD14. In situ hybridization experiments showed that, like the PsENOD3 and PsENOD14 genes, the PsNOD6 gene is only expressed in the infected cell type. The PsNOD6 gene is first expressed at the transition of the pre-fixation zone II into the interzone II–III (the amyloplast-rich zone preceding the fixation zone III), whereas the early nodulin genes PsENOD3 and PsENOD14 are already induced in the pre-fixation zone II. Thus these nodulin genes encoding homologous proteins are induced at consecutive stages of nodule development.

The expression of the late nodulin genes encoding leghaemoglobin precedes the expression of the late nodulin gene PsNOD6. Therefore these late nodulin genes have to be regulated by different mechanisms despite the fact they are expressed in the same cell type. This conclusion is consistent with the fact that PsNOD6 lacks one of the conserved regions occurring in the promoters of all other late nodulin genes studied.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Berg, JM: Potential metal-binding domains in nucleic acid binding proteins. Science 232: 485–487 (1986).

    PubMed  Google Scholar 

  2. Bisseling, T, van denBos, RC, vanKammen, A: The effect of ammonium nitrate on the synthesis of nitrogenase and the concentration of leghemoglobin in pea root nodules induced by Rhizobium leguminosarum. Biochim Biophys Acta 539: 1–11 (1978).

    PubMed  Google Scholar 

  3. Cock, JM, Brock, IW, Watson, AT, Swarup, R, Morby, AP, Cullimore, JV: Regulation of glutamine synthetase genes in leaves of Phaseolus vulgaris. Plant Mol Biol 17: 761–771 (1991).

    PubMed  Google Scholar 

  4. Cox, KH, Goldberg, RB: Analysis of plant gene expression. In: Shaw, CH (ed) Plant Molecular Biology: A Practical Approach, pp. 1–34. IRL Press, Oxford (1988).

    Google Scholar 

  5. DeBilly, F, Barker, DG, Gallusci, P, Truchet, G: Leghemoglobin gene transcription is triggered in a single cell layer in the indeterminate nitrogen-fixing root nodule of alfalfa. Plant J 1: 27–35 (1991).

    Google Scholar 

  6. deBruijn, F, Schell, J: Regulation of the plant genes specifically induced in developing and mature nitrogen-fixing nodules: cis-acting elements and trans-acting factors. In: Verma, DPS (ed) Control of Plant Gene Expression, pp. 241–257. CRC Press, Boca Raton, FL (1993).

    Google Scholar 

  7. de Maagd RA, Yang WC, Goossen-de Roo L, Mulders IHM, Roest HP, Spaink HP, Bisseling T, Lugtenberg BJJ: Down regulation of expression of the Rhizobium leguminosarum outer membrane protein gene ropA occurs abruptly in interzone II–III of pea nodules and can be uncoupled from nif gene activation. Submitted (1993).

  8. Devereux, J, Haeberli, P, Smithies, O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).

    PubMed  Google Scholar 

  9. deVries, SC, Springer, J, Wessels, JHG: Diversity of abundant mRNA sequences and patterns protein synthesis in etilated and greened pea seedlings. Planta 156: 129–135 (1982).

    Google Scholar 

  10. Franssen, H, Vijn, I, Yang, WC, Bisseling, T: Developmental aspects of the legume-Rhizobium symbiosis. Plant Mol Biol 19: 89–107 (1992).

    Article  PubMed  Google Scholar 

  11. Govers, F, Nap, JP, Moerman, M, Franssen, H, vanKammen, A, Bisseling, T: cDNA cloning and developmental expression of pea nodulin genes. Plant Mol Biol 8: 425–435 (1987).

    Google Scholar 

  12. Hanley, BA, Schuler, MA: Plant intron sequences: evidence for distinct groups of introns. Nucl Acids Res 16: 7159–7176 (1988).

    PubMed  Google Scholar 

  13. Joshi, CP: Putative polyadenylation signals in nuclear genes of higher plants: a compilation and analysis. Nucl Acids Res 15: 9627–9640 (1987).

    PubMed  Google Scholar 

  14. Kannenberg, EL, Brewin, NJ: Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxigen and pH. J Bacteriol 171: 4543–4548 (1989).

    PubMed  Google Scholar 

  15. Maxam, AM, Gilbert, W: A new method for sequencing DNA. Proc Natl Acad Sci USA 74: 560–562 (1977).

    PubMed  Google Scholar 

  16. Messing, J, Geraghty, D, Heidecker, G, Hu, NT, Kridl, J, Rubenstin, I: Plant gene structure. In: Kosuge, T, Meredith, C (eds) Genetic Engineering of plants, pp. 219–257. Plenum Press, New York (1983).

    Google Scholar 

  17. Nap JP: Nodulins in root nodule development. Ph. D. thesis, Wageningen Agricultural University, Netherlands (1988).

  18. Perotto S: Cell surface antigens in legume nodule development. Ph. D. thesis, University of East Anglia, UK (1992).

  19. Sambrook, JU, Fritsch, EF, Maniatis, T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  20. Scheres, B, vanEngelen, F, van derKnaap, E, van deWiel, C, vanKammen, A, Bisseling, T: Sequential induction of noduline gene expression in the developing pea nodule. Plant Cell 2: 687–700 (1990).

    Article  PubMed  Google Scholar 

  21. Scheres, B, van deWiel, C, Zalensky, A, Horvath, B, Spaink, H, vanEck, H, Zwartkruis, F, Volters, AM, Gloudemans, T, vanKammen, A, Bisseling, T: The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell 60: 281–294 (1990).

    Article  PubMed  Google Scholar 

  22. Vasse, J, DeBilly, F, Camut, S, Truchet, G: Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bact 172: 4295–4306 (1990).

    PubMed  Google Scholar 

  23. van deWiel, C, Scheres, B, Franssen, H, Lierop, MJ, vanLammeren, A, vanKammen, A, Bisseling, T: The early nodulin transcript ENOD2 is located in the nodule parenchma (inner cortex) of pea and soybean root nodules. EMBO J 9: 1–7 (1990).

    PubMed  Google Scholar 

  24. VonHeijne, G: A new method for predicting signal sequence cleavage sites. Nucl Acids Res 14: 4683–4690 (1986).

    PubMed  Google Scholar 

  25. Yang, WC, Horvath, B, vanKammen, A, Bisseling, T: In situ localization of Rhizobium messenger RNAs in pea root nodules in nifA and nifH localization. Mol Plant-Microbe Interact 4: 464–465 (1991).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kardailsky, I., Yang, WC., Zalensky, A. et al. 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 23, 1029–1037 (1993). https://doi.org/10.1007/BF00021817

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00021817

Key words

Navigation