Searching for regulators that interact with BELL1 transcription factor and control the legume-rhizobial symbiosis development

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Abstract


The development of nitrogen-fixing nodule, which is formed during legume-rhizobial symbiosis, requires the involvement of cell cycle regulators, phytohormones and homeodomain-containing transcription factors as well as other organogenesis processes. Along with homedomain-containing transcription factors from KNOX family, which participation in the control of nodule development has been studied recently, the role of transcription factors from BELL family in this process remains under-explored. At the same time, transcriptomic data for legumes shows an increase in the expression levels of genes encoding proteins of this family in the plant roots inoculated by Rhizobium. In this work we performed screening of сDNA library, which was generated from inoculated pea roots, using BELL1 protein in yeast two-hybrid system. As a result, we detected two interacting proteins, which are highly interesting for future examination. In the first case we discovered interaction between BELL1 and LysM-containing receptor-like kinase LYK9. Another identified regulator interacting with BELL1 became the glycine-rich protein A3, which may be involved in the regulation of defense reactions in plants and their resistance to phytopathogens. Transcriptomic analysis for pea roots has revealed high expression level of gene, which encodes this protein in the nodules, that may demonstrate its important role in symbiosis regulation.


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About the authors

Alexandra Vyacheslavovna Dolgikh

All-Russia Research Institute for Agricultural Microbiology; Saint Petersburg State University

Email: sqshadol@gmail.com
ORCID iD: 0000-0003-1845-9701
Scopus Author ID: 5719038282
ResearcherId: ABC-2930-2020

Russian Federation, 3 Podbelsky chausse, Pushkin, Saint Petersburg, 196608; Saint Petersburg

engineer

Elena A. Dolgikh

All-Russia Research Institute for Agricultural Microbiology

Author for correspondence.
Email: dol2helen@yahoo.com
ORCID iD: 0000-0002-5375-0943
SPIN-code: 4453-2060
Scopus Author ID: 6603496335
ResearcherId: G-6363-2017

Russian Federation, 3 Podbelsky chausse, Pushkin, Saint Petersburg, 196608

Dr. Sci. (Biol)

References

  1. Goodstein DM, Shu S, Howson R, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2011/11/22. 2012;40(Database issue): D1178–86. doi: 10.1093/nar/gkr944
  2. Chen H, Banerjee AK, Hannapel DJ. The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J. 2004;38(2):276–84. doi: 10.1111/j.1365-313X.2004.02048.x
  3. Azarakhsh M, Kirienko AN, Zhukov VA, et al. KNOTTED1-LIKE HOMEOBOX 3: a new regulator of symbiotic nodule development. J Exp Bot. 2015;66(22):7181–95. doi: 10.1093/jxb/erv414
  4. Di Giacomo E, Sestili F, Iannelli MA, et al. Characterization of KNOX genes in Medicago truncatula. Plant Mol Biol. 2008;67(1–2): 135–50. doi: 10.1007/s11103-008-9307-7
  5. Azarakhsh M, Lebedeva MA, Lutova LA. Identification and Expression Analysis of Medicago truncatula Isopentenyl Transferase Genes (IPTs) Involved in Local and Systemic Control of Nodulation. Front Plant Sci. 2018;9:1–11. doi: 10.3389/fpls.2018.00304
  6. Schiessl K, Lilley JLS, Lee T, et al. NODULE INCEPTION Recruits the Lateral Root Developmental Program for Symbiotic Nodule Organogenesis in Medicago truncatula. Curr Biol. 2019;29(21): 3657–3668.e5. doi: 10.1016/j.cub.2019.09.005
  7. Soyano T, Shimoda Y, Kawaguchi M, Hayashi M. A shared gene drives lateral root development and root nodule symbiosis pathways in Lotus. Science. 2019;366(6468):1021–1023. doi: 10.1126/science.aax2153
  8. Faulkner C. Receptor-mediated signaling at plasmodesmata. Front Plant Sci. 2013;4:521. doi: 10.3389/fpls.2013.00521
  9. Dolgikh AV, Rudaya ES, Dolgikh EA. Identification of BELL Transcription Factors Involved in Nodule Initiation and Development in the Legumes Pisum sativum and Medicago truncatula. Plants. 2020;9(12):1808. doi: 10.3390/plants9121808
  10. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–66. doi: 10.1093/nar/gkf436
  11. Yu G, Smith DK, Zhu H, et al. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017;8(1):28–36. doi: 10.1111/2041-210X.12628
  12. Bono J-J, Fliegmann J, Gough C, Cullimore J. Expression and function of the Medicago truncatula lysin motif receptor-like kinase (LysM-RLK) gene family in the legume–rhizobia symbiosis [Internet]. The Model Legume Medicago truncatula. 2020. p. 439–47. (Wiley Online Books). DOI: https://DOI.org/10.1002/9781119409144.ch55
  13. Gietz RD, Schiestl RH. Frozen competent yeast cells that can be transformed with high efficiency using the LiAc/SS carrier DNA/PEG method. Nat Protoc. 2007;2(1):1–4. doi: 10.1038/nprot.2007.17
  14. Beckmann BM. RNA interactome capture in yeast. Methods. 2017;118–119:82–92. doi: 10.1016/j.ymeth.2016.12.008
  15. Kreplak J, Madoui M-A, Cápal P, et al. A reference genome for pea provides insight into legume genome evolution. Nat Genet. 2019;51(9):1411–1422. doi: 10.1038/s41588-019-0480-1
  16. Leppyanen IV, Shakhnazarova VY, Shtark OY, et al. Receptor-Like Kinase LYK9 in Pisum sativum L. Is the CERK1-Like Receptor that Controls Both Plant Immunity and AM Symbiosis Development. Int J Mol Sci. 2017;19(1):8. doi: 10.3390/ijms19010008
  17. Tang H, Krishnakumar V, Bidwell S, et al. An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics. 2014;15(1):312. doi: 10.1186/1471-2164-15-312
  18. Goldberg T, Hecht M, Hamp T, et al. LocTree3 prediction of localization. Nucleic Acids Res. 2014;42(W1): W350–355. doi: 10.1093/nar/gku396
  19. Alves-Carvalho S, Aubert G, Carrère S, et al. Full-length de novo assembly of RNA-seq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights into root nodulation in this species. Plant J. 2015;84(1):1–19.
  20. Kirienko AN, Porozov YB, Malkov NV., et al. Role of a receptor-like kinase K1 in pea Rhizobium symbiosis development. Planta. 2018;248(5):1101–1120. doi: 10.1007/s00425-018-2944-4
  21. Cheval C, Samwald S, Johnston MG, et al. Chitin perception in plasmodesmata characterizes submembrane immune-signaling specificity in plants. Proc Natl Acad Sci. 2020;117(17):9621–9629. doi: 10.1073/pnas.1907799117
  22. Mangeon A, Junqueira RM, Sachetto-Martins G. Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav. 2010;5(2):99–104. doi: 10.4161/psb.5.2.10336
  23. Nakahara KS, Kitazawa H, Atsumi G, Choi SH, Suzuki Y, Uyeda I. Screening and analysis of genes expressed upon infection of broad bean with Clover yellow vein virus causing lethal necrosis. Virol J. 2011;8(1):355. doi: 10.1186/1743-422X-8-355

Supplementary files

Supplementary Files Action
1.
Fig. 1. Analysis of the interaction between the pea transcription factor BELL1 and proteins identified during screening libraries using yeast dihybrid system. The interaction was evaluated on selective SC medium without leucine, tryptophan and uracil (SC-LTU). Yeast growth on a selective medium shows the interaction of the studied proteins. As control, several pairs of vectors were used [pEXP32 / Krev1 and pEXP22 / RalGDS - wild type (wt), pEXP22 / RalGDS-m1 (m1 - mutant 1) and pEXP22 / RalGDS-m2 (m2 - mutant 2)] proposed by the manufacturer (Thermo Fisher Scientific) for study strong, weak interaction and undetectable interaction, respectively

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2.
Fig. 2. Phylogenetic tree illustrating the relationship between the protein identified during the screening of the library Psat5g112080 and LysM-RPK model bean Medicago truncatula

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3.
Fig. 3. Phylogenetic tree illustrating the relationship between the Psat4g107720 (URGI) protein detected during the library screening and glycine-proline-rich proteins of the A3 family of M. truncatula and peas

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4.
Fig. 4. Graphical illustration of data on the level of expression of genes encoding glycine-proline-rich proteins of the A3 family in pea nodules (cv. Cameor) at different stages development based on transcriptome analysis (RNA-seq) using the P. sativum v1 genome as a reference [17]. A - laying of nodules, B - the period of the beginning of flowering, C - 10 days after flowering

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