Skip to main content
SpringerLink
Log in

Regulatory Contexts in the 5'-Region of mRNA from Arabidopsis thaliana Plants and Their Role in Translation Efficiency

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

In this study, the polysome profiling method was used for the separation of mRNA depending on their loading by ribosomes into polysomal and monosomal fractions. Separation of pools of such mRNA and analysis of transcripts (mRNA), which are characterized by a constant level of transcription in a wide range of absolute values at all stages of plant ontogenesis and associated with each pool of mRNA due to RNA sequencing, allowed for obtaining an idea about the translational efficiency of individual mRNA. The consequent in silico analysis allowed performing a search for regulatory contexts in the 5'-region of mRNA of Arabidopsis thaliana plants that may be potentially important for efficient mRNA translation. The results of the study revealed that pyrimidine dinucleotides and motifs are characteristic of a 5'-untranslated mRNA region with high translation efficiency, whereas purine dinucleotides and motifs are associated with transcripts with low translational efficiency.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

REFERENCES

  1. Kawaguchi, R., mRNA sequence features that contribute to translational regulation in Arabidopsis,Nucleic Acids Res., 2005, vol. 33, p. 955. https://doi.org/10.1093/nar/gki240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Sablok, G., Powell, J.J., and Kazan, K., Emerging roles and landscape of translating mRNAs in plants, Front. Plant Sci., 2017, vol. 8: 1443. https://doi.org/10.3389/fpls.2017.01443

    Article  PubMed  PubMed Central  Google Scholar 

  3. Goldenkova-Pavlova, I., Pavlenko, O., Mustafaev, O., Deyneko, I., Kabardaeva, K., and Tyurin, A., Computational and experimental tools to monitor the changes in translation efficiency of plant mRNA on a genome-wide scale: advantages, limitations, and solutions, Int. J. Mol. Sci., 2018, vol. 20, p. 33. https://doi.org/10.3390/ijms20010033

    Article  CAS  PubMed Central  Google Scholar 

  4. Kabardaeva, K.V., Tyurin, A.A., Pavlenko, O.S., Gra, O.A., Deyneko, I.V., Kouchoro, F., Mustafaev, O.N., and Goldenkova-Pavlova, I.V., Fine tuning of translation: a complex Web of mechanisms and its relevance to plant functional genomics and biotechnology, Russ. J. Plant Physiol., 2019, vol. 66, p. 835. https://doi.org/10.1134/S1021443719060074

    Article  CAS  Google Scholar 

  5. Kozak, M., How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell, 1978, vol. 15, p. 1109. https://doi.org/10.1016/0092-8674(78)90039-9

    Article  CAS  PubMed  Google Scholar 

  6. Mustroph, A., Zanetti, M.E., Jang, C.J.H., Holtan, H.E., Repetti, P.P., Galbraith, D.W., and Bailey-Serres, J., Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis,Proc. Natl. Acad. Sci. USA, 2009, vol. 106, p. 18843. https://doi.org/10.1073/pnas.0906131106

    Article  PubMed  Google Scholar 

  7. Bai, B., Peviani, A., van der Horst, S., Gamm, M., Snel, B., Bentsink, L., and Hanson, J., Extensive translational regulation during seed germination revealed by polysomal profiling, New Phytol., 2017, vol. 214, p. 233. https://doi.org/10.1111/nph.14355

    Article  CAS  PubMed  Google Scholar 

  8. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R.S., and Weissman, J.S., Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling, Science, 2009, vol. 324, p. 218. https://doi.org/10.1126/science.1168978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Baerenfaller, K., Grossmann, J., Grobei, M.A., Hull, R., Hirsch-Hoffmann, M., Yalovsky, S., Zimmermann, P., Grossniklaus, U., Gruissem, W., and Baginsky, S., Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics, Science, 2008, vol. 320, p. 938. https://doi.org/10.1126/science.1157956

    Article  CAS  PubMed  Google Scholar 

  10. Baerenfaller, K., Massonnet, C., Walsh, S., Baginsky, S., Buhlmann, P., Hennig, L., Hirsch-Hoffmann, M., Howell, K.A., Kahlau, S., Radziejwoski, A., Russenberger, D., Rutishauser, D., Small, I., Stekhoven, D., Sulpice, R., et al., Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit, Mol. Syst. Biol., 2012, vol. 8, p. 606. https://doi.org/10.1038/msb.2012.39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Qi, W., Schlapbach, R., and Rehrauer, H., RNA-Seq data analysis: from raw data quality control to differential expression analysis, Methods Mol. Biol., 2017, vol. 1669, p. 295. https://doi.org/10.1007/978-1-4939-7286-9_23

    Article  CAS  PubMed  Google Scholar 

  12. Larsson, O., Sonenberg, N., and Nadon, R., Identification of differential translation in genome wide studies, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, p. 21487. https://doi.org/10.1073/pnas.1006821107

    Article  PubMed  Google Scholar 

  13. Crooks, G.E., WebLogo: a sequence logo generator, Genome Res., 2004, vol. 14, p. 1188. https://doi.org/10.1101/gr.849004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.-R., Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis,Plant Physiol., 2005, vol. 139, p. 5. https://doi.org/10.1104/pp.105.063743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhang, X., Rosen, B.D., Tang, H., Krishnakumar, V., and Town, C.D., Polyribosomal RNA-Seq reveals the decreased complexity and diversity of the Arabidopsis translatome, PLoS One, 2015, vol. 10: e0117699. https://doi.org/10.1371/journal.pone.0117699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hsu, P.Y., Calviello, L., Wu, H.L., Li, F.W., Rothfels, C.J., Ohler, U., and Benfey, P.N., Super-resolution ribosome profiling reveals unannotated translation events in Arabidop-sis,Proc. Natl. Acad. Sci. USA, 2016, vol. 113: e7126. https://doi.org/10.1073/pnas.1614788113

    Article  CAS  PubMed  Google Scholar 

  17. Kim, Y., Lee, G., Jeon, E., Sohn, E.J., Lee, Y., Kang, H., Lee, D.W., Kim, D.H., and Hwang, I., The immediate upstream region of the 5'-UTR from the AUG start codon has a pronounced effect on the translational efficiency in Arabidopsis thaliana,Nucleic Acids Res., 2014, vol. 42, p. 485. https://doi.org/10.1093/nar/gkt864

    Article  CAS  PubMed  Google Scholar 

  18. Kanoria, S. and Burma, P.K., A 28 nt long synthetic 5′UTR (synJ) as an enhancer of transgene expression in dicotyledonous plants, BMC Biotechnol., 2012, vol. 12, p. 85. https://doi.org/10.1186/1472-6750-12-85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tyurin, A.A., Kabardaeva, K.V., Gra, O.A., Mustafaev, O.N., Sadovskaya, N.S., Pavlenko, O.S., and Goldenkova-Pavlova, I.V., Efficient expression of a heterologous gene in plants depends on the nucleotide composition of mRNA’s 5′-region, Russ. J. Plant Physiol., 2016, vol. 63, pp. 511.

    Article  CAS  Google Scholar 

  20. Kozak, M., Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes, Cell, 1986, vol. 44, p. 283. https://doi.org/10.1016/0092-8674(86)90762-2

    Article  CAS  PubMed  Google Scholar 

  21. Tzeng, T.Y., Kong, L.R., Chen, C.H., Shaw, C.C., and Yang, C.H., Overexpression of the lily p70s6k gene in Arabidopsis affects elongation of flower organs and indicates TOR-dependent regulation of AP3, PI and SUP translation, Plant Cell Physiol., 2009, vol. 50, p. 1695. https://doi.org/10.1093/pcp/pcp114

    Article  CAS  PubMed  Google Scholar 

  22. Ortega, J.L., Wilson, O.L., and Sengupta-Gopalan, C., The 5′ untranslated region of the soybean cytosolic glutamine synthetase β1 gene contains prokaryotic translation initiation signals and acts as a translational enhancer in plants, Mol. Genet. Genomics, 2012, vol. 287, p. 881. https://doi.org/10.1007/s00438-012-0724-6

    Article  CAS  PubMed  Google Scholar 

  23. Liu, M.J., Wu, S., Chen, H.M., and Wu, S.H., Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis, Mol. Syst. Biol., 2012, vol. 8, p. 566. https://doi.org/10.1038/msb.2011.97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Agarwal, P., Garg, V., Gautam, T., Pillai, B., Kanoria, S., and Burma, P.K., A study on the influence of different promoter and 5′UTR (URM) cassettes from Arabidopsis thaliana on the expression level of the reporter gene β glucuronidase in tobacco and cotton, Transgenic Res., 2014, vol. 23, p. 351.

    Article  CAS  Google Scholar 

  25. Nakagawa, S., Niimura, Y., Gojobori, T., Tanaka, H., and Miura, K.I., Diversity of preferred nucleotide sequences around the translation initiation codon in eukaryote genomes, Nucleic Acids Res., 2007, vol. 36, p. 861. https://doi.org/10.1093/nar/gkm1102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gupta, P., Rangan, L., Ramesh, T.V., and Gupta, M., Comparative analysis of contextual bias around the translation initiation sites in plant genomes, J. Theor. Biol., 2016, vol. 404, p. 303. https://doi.org/10.1016/j.jtbi.2016.06.015

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the Russian Foundation for Basic Research (project no. 17-04-00783).

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127276, Moscow, Russia

    K. V. Kabardaeva, A. A. Turin, F. Kouchoro, I. V. Deineko, V. S. Fadeev & I. V. Goldenkova-Pavlova

  2. Genetic Resources Institute, National Academy of Sciences of Azerbaijan, AZ1106, Baku, Azerbaijan

    O. N. Mustafaev

Authors
  1. K. V. Kabardaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Turin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Kouchoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. N. Mustafaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. I. V. Deineko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. S. Fadeev
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. V. Goldenkova-Pavlova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. V. Goldenkova-Pavlova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies involving animals or human participants performed by any of the authors.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

Additional information

Translated by V. Mittova

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kabardaeva, K.V., Turin, A.A., Kouchoro, F. et al. Regulatory Contexts in the 5'-Region of mRNA from Arabidopsis thaliana Plants and Their Role in Translation Efficiency. Russ J Plant Physiol 67, 425–434 (2020). https://doi.org/10.1134/S1021443720030139

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443720030139

Keywords:

Search

Navigation