, Volume 255, Issue 5, pp 1443–1459 | Cite as

Early nodule senescence is activated in symbiotic mutants of pea (Pisum sativum L.) forming ineffective nodules blocked at different nodule developmental stages

  • Tatiana A. Serova
  • Anna V. Tsyganova
  • Viktor E. Tsyganov
Original Article


Plant symbiotic mutants are useful tool to uncover the molecular-genetic mechanisms of nodule senescence. The pea (Pisum sativum L.) mutants SGEFix-1 (sym40), SGEFix-3 (sym26), and SGEFix-7 (sym27) display an early nodule senescence phenotype, whereas the mutant SGEFix-2 (sym33) does not show premature degradation of symbiotic structures, but its nodules show an enhanced immune response. The nodules of these mutants were compared with each other and with those of the wild-type SGE line using seven marker genes that are known to be activated during nodule senescence. In wild-type SGE nodules, transcript levels of all of the senescence-associated genes were highest at 6 weeks after inoculation (WAI). The senescence-associated genes showed higher transcript abundance in mutant nodules than in wild-type nodules at 2 WAI and attained maximum levels in the mutant nodules at 4 WAI. Immunolocalization analyses showed that the ethylene precursor 1-aminocyclopropane-1-carboxylate accumulated earlier in the mutant nodules than in wild-type nodules. Together, these results showed that nodule senescence was activated in ineffective nodules blocked at different developmental stages in pea lines that harbor mutations in four symbiotic genes.


Nodulation Symbiosis Symbiosomes Ethylene Sanctions Programmed cell death 



Abscisic acid




Weeks after inoculation


Days after inoculation



This work was supported by the Russian Science Foundation [grant number 16-16-10035]. The research was performed using equipment of the Core Centrum “Genomic Technologies, Proteomics and Cell Biology” in ARRIAM, and the “Molecular and Cell Technologies” Research Resource Centre at Saint-Petersburg State University. Jennifer Smith, PhD, and Robert McKenzie, PhD, from Edanz Group ( edited the English version of a draft of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest

Supplementary material

709_2018_1246_MOESM1_ESM.pdf (3.9 mb)
ESM 1 (PDF 4038 kb)


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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Tatiana A. Serova
    • 1
  • Anna V. Tsyganova
    • 1
  • Viktor E. Tsyganov
    • 1
  1. 1.All-Russia Research Institute for Agricultural Microbiology, Laboratory of Molecular and Cellular BiologySaint-PetersburgRussia

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