Transcriptomic analysis of sym28 and sym29 supernodulating mutants of pea (Pisum sativum L.) under complex inoculation with beneficial microorganisms

  • Vladimir Zhukov Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-2411-9191
  • Evgeny Zorin Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-5666-3020
  • Aleksandr Zhernakov Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-8961-9317
  • Alexey Afonin Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-8530-0226
  • Gulnar Akhtemova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-7957-3693
  • Andrej Bovin Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-4061-435X
  • Aleksandra Dolgikh Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-1845-9701
  • Artemii Gorshkov Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-7296-0188
  • Emma Gribchenko Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-1538-5527
  • Kira Ivanova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-9119-065X
  • Anna Kirienko Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-2519-306X
  • Anna Kitaeva Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-7873-6737
  • Marina Kliukova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-1119-5512
  • Olga Kulaeva Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-2687-9693
  • Pyotr Kusakin Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-2795-515X
  • Irina Leppyanen Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-2158-0855
  • Olga Pavlova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-0528-5618
  • Daria Romanyuk Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-9576-1256
  • Elizaveta Rudaya Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-3081-9880
  • Tatiana Serova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-7236-1003
  • Oksana Shtark Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-3656-4559
  • Anton Sulima Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-2300-857X
  • Anna Tsyganova Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-3505-4298
  • Ekaterina Vasileva Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0001-5599-0361
  • Elena Dolgikh Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0002-5375-0943
  • Viktor Tsyganov Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation https://orcid.org/0000-0003-3105-8689
  • Igor Tikhonovich Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Shosse Podbel'skogo, 3, Saint Petersburg, 190608, Russian Federation; Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-8968-854X

Abstract

The garden pea (Pisum sativum L.), like most members of Fabaceae family, is capable of forming symbioses with beneficial soil microorganisms such as nodule bacteria (rhizobia), arbuscular mycorrhizal (AM) fungi and plant growth promoting bacteria (PGPB). The autoregulation of nodulation (AON) system is known to play an important role in controlling both the number of nodules and the level of root colonization by AM via root-to-shoot signaling mediated by CLAVATA/ESR-related (CLE) peptides and their receptors. In the pea, mutations in genes Sym28 (CLV2-like) and Sym29 (CLV1-like), which encode receptors for CLE peptides, lead to the supernodulation phenotype, i.e., excessive nodule formation. The aim of the present study was to analyze the response of pea cv. ‘Frisson’ (wild type) and mutants P64 (sym28) and P88 (sym29) to complex inoculation with rhizobia, AM fungi and PGPB, with regard to biomass accumulation, yield and transcriptomic alterations. The plants were grown in quartz sand for 2 and 4 weeks after inoculation with either rhizobia (Rh) or complex inoculation with Rh + AM, Rh + PGPB, and Rh+AM+PGPB, and the biomass and yield were assessed. Transcriptome sequencing of whole shoots and roots was performed using a modified RNAseq protocol named MACE (Massive Analysis of cDNA Ends). In the experimental conditions, P88 (sym29) plants demonstrated the best biomass accumulation and yield, as compared to the wild type and P64 (sym28) plants, whereas P64 (sym28) had the lowest rate of biomass and seed yield. The transcriptome analysis showed that both supernodulating mutants more actively responded to biotic and abiotic factors than the wild-type plants and demonstrated increased expression of genes characteristic to late stages of nodule development. The roots of P64 (sym28) plants responded to AM+Rh treatment with upregulation of genes encoding plastid proteins, which can be connected with the activation of carotenoid biosynthesis (namely, the non-mevalonate pathway that takes place in root plastids). The more active response to symbionts in P88 (sym29) plants, as compared to cv. ‘Frisson’, was associated with counterregulation of transcripts involved in chloroplast functioning and development in leaves, which accompanies successful plant development in symbiotic conditions. Finally, the effect of retardation of plant aging upon mycorrhization on a transcriptomic level was recorded for cv. ‘Frisson’ but not for P64 (sym28) and P88 (sym29) mutants, which points towards its possible connection with the AON system. The results of this work link the plant’s autoregulation with the responsiveness to inoculation with beneficial soil microorganisms.

Keywords:

RNAseq, transcriptomics, arbuscular mycorrhiza, nodule bacteria, complex inoculation, autoregulation of nodulation, garden pea

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Published
2021-11-12
How to Cite
Zhukov, V., Zorin, E., Zhernakov, A., Afonin, A., Akhtemova, G., Bovin, A., Dolgikh, A., Gorshkov, A., Gribchenko, E., Ivanova, K., Kirienko, A., Kitaeva, A., Kliukova, M., Kulaeva, O., Kusakin, P., Leppyanen, I., Pavlova, O., Romanyuk, D., Rudaya, E., Serova, T., Shtark, O., Sulima, A., Tsyganova, A., Vasileva, E., Dolgikh, E., Tsyganov, V., & Tikhonovich, I. (2021). Transcriptomic analysis of <em>sym28</em> and <em>sym29</em> supernodulating mutants of pea (<em>Pisum sativum</em&gt; L.) under complex inoculation with beneficial microorganisms. Biological Communications, 66(3), 181–197. https://doi.org/10.21638/spbu03.2021.301
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Full communications

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