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Double mutant analysis of sequential functioning of pea (Pisum sativum L.) genes Sym13, Sym33, and Sym40 during symbiotic nodule development

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Russian Journal of Genetics: Applied Research

Abstract

Two double mutants carrying pea symbiotic gene pairs sym13, sym40 and sym33, respectively, were constructed using single mutants blocked at different nodule developmental stages: E135F (sym13), SGE-Fix−-1 (sym40) and SGEFix−-2 (sym33). The epistasis of the mutant allele sym40 over the mutant allele sym13 and sym33 over sym40 was shown with respect to nodule histological and ultrastructural organization. Thus, the proposed earlier sequential functioning of genes during infection process Sym33 → Sym40 → Sym13 has been confirmed.

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References

  • Avery, L. and Wasserman, S., Ordering Gene Function: the Interpretation of Epistasis in Regulatory Hierarchies, Trends Genet., 1992, vol. 8, pp. 312–316.

    PubMed  CAS  Google Scholar 

  • Bhatia, C.R., Nichterlein, K., and Maluszynski, M., Mutations Affecting Nodulation in Grain Legumes and Their Potential in Sustainable Cropping Systems, Euphytica, 2001, vol. 120, pp. 415–432.

    Article  Google Scholar 

  • Borisov, A.Y., Morzhina, E.V., Kulikova, O.A., et al., New Symbiotic Mutants of Pea (Pisum sativum L.) Affecting Either Nodule Initiation or Symbiosome Development, Symbiosis, 1992, vol. 14, pp. 297–313.

    Google Scholar 

  • Borisov, A.Y., Rozov, S.M., Tsyganov, V.E., et al., Sequential Functioning of Sym-13 and Sym-31, Two Genes Affecting Symbiosome Development in Root Nodules of Pea (Pisum sativum L.), Mol. Gen. Genet., 1997, vol. 254, pp. 592–598.

    Article  PubMed  CAS  Google Scholar 

  • Borisov, A.Y., Danilova, T.N., Koroleva, T.A., et al., Pea (Pisum sativum L.) Regulatory Genes Controlling Development of Nitrogen-Fixing Nodule and Arbuscular Mycorrhiza: Fundamentals and Application, Biologia, 2004, vol. 59,suppl., pp. 137–144.

    CAS  Google Scholar 

  • Brewin, N.J., Plant Cell Wall Remodelling in the Rhizobium-Legume Symbiosis, Critic. Rev. Plant Sci., 2004, vol. 23, pp. 293–316.

    Article  CAS  Google Scholar 

  • Caetano-Anollés, G. and Gresshoff, P.M., Plant Genetic Control of Nodulation, Annu. Rev. Microbiol., 1991, vol. 45, pp. 345–382.

    Article  PubMed  Google Scholar 

  • Guinel, F.C. and Geil, R.D., A Model for the Development of the Rhizobial and Arbuscular Mycorrhizal Symbiosis in Legumes and Its Use to Understand the Roles of Ethylene in the Establishment of These Two Symbiosis, Can. J. Bot., 2002, vol. 80, pp. 695–720.

    Article  CAS  Google Scholar 

  • Kneen, B.E., LaRue, T.A., Hirsch, A.M., et al., Sym13, A Gene Conditioning Ineffective Nodulation in Pisum sativum, Plant Physiol., 1990, vol. 94, pp. 899–905.

    Article  PubMed  CAS  Google Scholar 

  • Koornnef, M., Alonso-Blanco, C., Peeters, A.J.M., et al., Genetic Control of Flowering Time in Arabidopsis, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1998a, vol. 49, pp. 345–370.

    Article  Google Scholar 

  • Koornnef, M., Alonso-Blanco, C., de Vries, H.B., et al., Genetic Interactions among Late-Flowering Mutants in Arabidopsis, Genetics, 1998b, vol. 148, pp. 885–892.

    Google Scholar 

  • Kosterin, O.E. and Rozov, S.M., Mapping of the New Mutation Blb and the Problem of Integrity of Linkage Group I, Pisum Genet., 1993, vol. 25, pp. 27–31.

    Google Scholar 

  • Morzhina, E.V., Tsyganov, V.E., Borisov, A.Y., et al., Four Developmental Stages Identified by Genetic Dissection of Pea (Pisum sativum L.) Root Nodule Morphogenesis, Plant Sci., 2000, vol. 155, pp. 75–83.

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd, G.E.D. and Downie, J.A., Calcium, Kinases and Nodulation Signalling in Legumes, Mol. Cell Biol., 2004, vol. 5, pp. 566–576.

    CAS  Google Scholar 

  • Oldroyd, G.E.D. and Downie, J.A., Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 519–546.

    Article  PubMed  CAS  Google Scholar 

  • Parker, J.S., Cavell, A.C., Dolan, L., et al., Genetic Interactions during Root Hair Morphogenesis in Arabidopsis, Plant Cell, 2000, vol. 12, pp. 1961–1974.

    Article  PubMed  CAS  Google Scholar 

  • Rathbun, E.A., Naldrett, M.J., and Brewin, N.J., Identification of a Family of Extension-Like Glycoproteins in the Lumen of Rhizobium-Induced Infection Threads in Pea Root Nodules, Mol. Plant-Microbe Interact., 2002, vol. 15, pp. 350–359.

    Article  PubMed  CAS  Google Scholar 

  • Safronova, V.I. and Novikova, N.I., Comparison of Two Methods for Root Nodule Bacteria Preservation: Lyophilization and Liquid Nitrogen Freezing, J. Microbiol. Methods, 1996, vol. 24, pp. 231–237.

    Article  Google Scholar 

  • Tsyganov, V.E., Morzhina, E.V., Stefanov, S.Y., et al., The Pea (Pisum sativum L.) Genes sym33 and sym40 Control Infection Thread Formation and Root Nodule Functioning, Mol. Gen. Genet., 1998, vol. 259, pp. 491–503.

    Article  PubMed  CAS  Google Scholar 

  • Tsyganov, V.E., Voroshilova, V.A., Priefer, U.B., et al., Genetic Dissection of the Initiation of the Infection Process and Nodule Tissue Development in the Rhizobium-Pea (Pisum sativum L.) Symbiosis, Ann. Bot. (Lond.), 2002, vol. 89, pp. 357–366.

    Article  CAS  Google Scholar 

  • Tsyganov, V.E., Voroshilova, V.A., Herrera-Cervera, J.A., et al., Developmental Down-Regulation of Rhizobial Genes as a Function of Symbiosome Differentiation in Symbiotic Root Nodules of Pisum sativum L., New Phytol., 2003, vol. 159, pp. 521–530.

    Article  CAS  Google Scholar 

  • Tsyganova, A.V., Tsyganov, V.E., Findlay, K.K., et al., Distribution of Legume Arabinogalactanprotein-Extensin (AGPE) Glycoproteins in Symbiotically Defective Pea Mutants with Abnormal Infection Threads, Tsitologiia, 2009, vol. 51, no. 1, pp. 53–62.

    PubMed  CAS  Google Scholar 

  • Voroshilova, V.A., Boesten, B., Tsyganov, V.E., et al., Effect of Mutations in Pisum sativum L. Genes (sym13, sym31, sym33, sym40) Blocking Different Stages of Nodule Development on the Expression of Late Symbiotic Genes in Rhizobium leguminosarum bv. viciae, Mol. Plant-Microbe Interact., 2001, vol. 14, pp. 471–476.

    Article  PubMed  CAS  Google Scholar 

  • Walker, S.A., Viprey, V., and Downie, J.A., Dissection of Nodulation Signaling using Pea Mutants Defective for Calcium Spiking Induced by Nod Factors and Chitin Oligomers, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 13413–13418.

    Article  PubMed  CAS  Google Scholar 

  • Wang, T.L., Wood, E.A., and Brewin, N.J., Growth Regulators, Rhizobium and Nodulation of Peas, Planta, 1982, vol. 155, pp. 345–349.

    Article  CAS  Google Scholar 

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Author notes

  1. E. V. Seliverstova

    Present address: I.M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, pr. Toreza 44, Saint Petersburg, 194223, Russia

  2. V. K. Lebskii

    Present address: Centro de Investigaciones Biológicas del Noroeste, S.C. Km. 1 Carretera a San Juan de La Costa “EL COMITAN” Apdo., Postal 128, La Paz, BCS 23097, México

Authors and Affiliations

  1. All-Russia Research Institute for Agricultural Microbiology, Podbelsky chaussee 3, Pushkin 8, Saint Petersburg, 196608, Russia

    V. E. Tsyganov, E. V. Seliverstova, V. A. Voroshilova, A. V. Tsyganova, Z. B. Pavlova, V. K. Lebskii, A. Yu. Borisov & I. A. Tikhonovich

  2. John Innes Centre, Norwich Research Park, Colney Lane, Norwich, NR4 7UH, UK

    N. J. Brewin

Authors
  1. V. E. Tsyganov
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  2. E. V. Seliverstova
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  3. V. A. Voroshilova
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  4. A. V. Tsyganova
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  5. Z. B. Pavlova
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  6. V. K. Lebskii
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  7. A. Yu. Borisov
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  8. N. J. Brewin
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  9. I. A. Tikhonovich
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Additional information

Original Russian Text © V.E. Tsyganov, E.V. Seliverstova, V.A. Voroshilova, A.V. Tsyganova, Z.B. Pavlova, V.K. Lebskii, A.Yu. Borisov, N.J. Brewin, I.A. Tikhonovich, 2010, published in Ekologicheskaya Genetika, 2010, Vol. 8, No. 2, pp. 3–8.

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Tsyganov, V.E., Seliverstova, E.V., Voroshilova, V.A. et al. Double mutant analysis of sequential functioning of pea (Pisum sativum L.) genes Sym13, Sym33, and Sym40 during symbiotic nodule development. Russ J Genet Appl Res 1, 343–348 (2011). https://doi.org/10.1134/S2079059711050145

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  • DOI: https://doi.org/10.1134/S2079059711050145

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