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Predicting Characteristics of the Potentially Binding Sites for miRNA in the mRNA of the TCP Transcription Factor Genes of Plants

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Abstract

The expression of the TCP transcription factor family genes depends on miRNA, whose effect on the translation of their mRNA is poorly studied. Interactions between miRNA and mRNA were studied with the MirTarget program, which allows estimating of quantitative characteristics of binding of the whole nucleotide sequence of miRNA to mRNA. The analysis of binding of 125 miRNAs to mRNAs of 28 genes of the TCP family of Triticum aestivum L. revealed eight target genes for miR319-3p, miR444a-3p, miR5086-5p, miR9666a-3p, and miR9780-3p. miRNA binding sites in mRNA of the TCP family genes of T. aestivum were located in the CDS only. Only 12 of 22 mRNAs of the ТСР family genes of Oryza sativa L. bounded to the miR1437b-5p, miR1846a-5p, miR1848-5p, miR1858a-5p, miR1858b-5p, miR1861d-5p, miR1861h-5p, miR2102-3p, miR2102-5p, miR2919, miR2925-5p, miR319a-3, miR408-3p, miR5075-3p, and miR5819-5p out of 738 miRNAs in total. miRNA binding sites were located in the 5'UTR and CDS regions of mRNAs of the TCP family genes of O. sativa. Only 10 of 46 TCP family genes of Zea mays L. were shown to be targets for the miR164g-3p, miR164h-5p, miR166a-5p, miR168a-5p, miR171d-5p, miR399d-3p, and miR408a-3p out of 325 miRNAs of Z. mays. The zma-miR166a-5p was bound to mRNAs of the genes GRMZM2G031905_P01, GRMZM2G055024_P01, GRMZM2G062711_P01, and GRMZM2G170232_P01. Two miRNAs were shown to bind to mRNAs of the genes AC213524.3_FGP003, AC233950.1_FGP002, and GRMZM2G034638_P01. Only one miRNA was bound to mRNAs of the genes GRMZM2G035944_P01, AC190734.2_FGP003, and AC205574.3_FGP006. miRNA binding sites were located in the 5'UTR and CDS regions of mRNAs of the TCP family genes of Z. mays. Ten of 27 TCP family genes of Arabidopsis thaliana (L.) Heynh. were shown to be targets for the miR319-3р, miR4228-5p, miR4228-3p, miR5021-5p, miR5658-5p, and miR8181-5p out of 429 miRNAs of A. thaliana. mRNAs of the AT1G53230 and AT2G31070 genes had binding sites for the miR319c-3p, miR5021-5p, and miR5658-5p, while mRNA of the AT3G15030 gene had binding site for the miR319a-3p and miR4228-3p. Two miRNAs bounded to mRNAs of the genes AT1G69690, AT3G02150, and AT3G47620. One miRNA bounded to mRNAs of the genes AT1G30210, AT4G18390, and AT5G08330. miRNA binding sites were located in the 5'UTR, CDS and 3'UTR regions of mRNA of the TCP gene family of A. thaliana. mRNAs of six groups of the TCP family genes had binding sites for the miR319-3p, miR444a-3p, miR5021-5p, miR5658-5p, and miR2102-5p, which encode the oligopeptides QRGPLQS, STSETS, SSSSSS, HHHHHH, GGGGGG, and AAAAAA conservative in the TCP family proteins of different plant species. Quantitative characteristics of miRNA binding to mRNAs of plant transcription factors of the TCP family, which participate in regulation of growth and development of plants, have been predicted.

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REFERENCES

  1. Li, S., The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development, Plant Signal. Behav., 2015, vol. 10: e1044192. https://doi.org/10.1080/15592324.2015.1044192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Manassero, N., Viola, I., Welchen, E., and Gonzalez, D., TCP transcription factors: architectures of plant form, Biomol. Concepts, 2013, vol. 4, p. 111. https://doi.org/10.1515/bmc-2012-0051

    Article  CAS  PubMed  Google Scholar 

  3. Sengupta, A. and Hileman, L., Novel traits, flower symmetry, and transcriptional autoregulation: new hypotheses from bioinformatic and experimental data, Front. Plant Sci., 2018, vol. 9: 1561. https://doi.org/10.3389/fpls.2018.01561

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mart, M. and Cubas, P., TCP genes: a family snapshot ten years later, Trends Plant Sci., 2010, vol. 15, p. 31. https://doi.org/10.1016/j.tplants.2009.11.003

    Article  CAS  Google Scholar 

  5. Reinhart, B., Weinstein, E., Rhoades, M., Bartel, B., and Bartel, D., MicroRNAs in plants, Genes Dev., 2002, vol. 16, p. 1616. https://doi.org/10.1101/gad.1004402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Rogers, K. and Chen, X., Biogenesis, turnover, and mode of action of plant microRNAs, Plant Cell, 2013, vol. 25, p. 2383. https://doi.org/10.1105/tpc.113.113159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., and Dharmasiri, N., A plant miRNA contributes to antibacterial resistance by repressing auxin signaling, Scien-ce, 2006, vol. 312, p. 436. https://doi.org/10.1126/science.aae0382

    Article  CAS  Google Scholar 

  8. Zhang, L., Zheng, Y., Jagadeeswaran, G., Li, Y., Gowdu, K., and Sunkar, R., Identification and temporal expression analysis of conserved and novel microRNAs in Sorghum,Genomics, 2011, vol. 98, p. 460. https://doi.org/10.1016/j.ygeno.2011.08.005

    Article  CAS  PubMed  Google Scholar 

  9. Phillips, J.R., Dalmay, T., and Bartels, D., The role of small RNAs in abiotic stress, FEBS Lett., 2007, vol. 581, p. 3592. https://doi.org/10.1016/j.febslet.2007.04.007

    Article  CAS  PubMed  Google Scholar 

  10. Yan, Y., Wang, H., Hamera, S., Chen, X., and Fang, R., miR444a has multiple functions in the rice nitrate-signaling pathway, Plant J., 2014, vol. 78, no. 1, p. 44. https://doi.org/10.1111/tpj.12446

    Article  CAS  PubMed  Google Scholar 

  11. Palatnik, J.F., Wollmann, H., Schommer, C., Schwab, R., Boisbouvier, J., Rodriguez, R., Warthmann, N., Allen, E., Dezulian, T., Huson, D., Carrington, J.C., and Weigel, D., Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319, Dev. Cell, 2007, vol. 13, no. 1, p. 115. https://doi.org/10.1016/j.devcel.2007.04.012

    Article  CAS  PubMed  Google Scholar 

  12. Tomotsugu, K., Fumihiko, S., and Masaru, O., Roles of miR319 and TCP transcription factors in leaf development, Plant Physiol., 2017, vol. 175, p. 874. https://doi.org/10.1104/pp.17.00732

    Article  CAS  Google Scholar 

  13. Li, Z., An, X., Zhu, T., Yan, T., Wu, S., Tian, Y., Li, J., and Wan, X., Discovering and constructing ceRNA-miRNA-target gene regulatory networks during anther development in maize, Int. J. Mol. Sci., 2019, vol. 20, no. 14: e3480. https://doi.org/10.3390/ijms20143480

    Article  CAS  PubMed  Google Scholar 

  14. Yusuf, N.H., Ong, W.D., Redwan, R.M., Latip, M.A., and Kumar, S.V., Discovery of precursor and mature microRNAs and their putative gene targets using high-throughput sequencing in pineapple (Ananas comosus var. comosus), Gene, 2016, vol. 571, p. 71. https://doi.org/10.1016/j.gene.2015.06.050

    Article  CAS  Google Scholar 

  15. Wu, F.Y., Tang, C.Y., Guo, Y.M., Yang, M.K., Yang, R.W., Lu, G.H., and Yang, Y.H., Comparison of miRNAs and their targets in seed development between two maize inbred lines by high-throughput sequencing and degradome analysis, PLoS One, 2016, vol. 11, no. 7: e0159810. https://doi.org/10.1371/journal.pone.0159810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. De Boer, K., Melser, S., Sperschneider, J., Kamphuis, L.G., Garg, G., Gao, L.L., Frick, K., and Singh, K.B., Identification and profiling of narrow-leafed lupin (Lupinus angustifolius) microRNAs during seed development, BMC Genomics, 2019, vol. 20, no. 1: 135. https://doi.org/10.1186/s12864-019-5521-8

    Article  Google Scholar 

  17. López-Ruiz, B.A., Juárez-González, V.T., Sandoval-Zapotitla, E., and Dinkova, T.D., Development-related miRNA expression and target regulation during staggered in vitro plant regeneration of Tuxpeño VS‑53--5 maize cultivar, Int. J. Mol. Sci., 2019, vol. 20, no. 9: e2079. https://doi.org/10.3390/ijms20092079

  18. Wang, Y., Peng, M., Wang, W., Chen, Y., He, Z., Cao, J., Lin, Z., Yang, Z., Gong, M., and Yin, Y., Verification of miRNAs in ginseng decoction by high-throughput sequ-encing and quantitative real-time PCR, Heliyon, 2019, vol. 5, no. 4: e01418. https://doi.org/10.1016/j.heliyon.2019.e01418

    Article  PubMed  PubMed Central  Google Scholar 

  19. Aydinoglu, F. and Lucas, S.J., Identification and expression profiles of putative leaf growth related microRNAs in maize (Zea mays L.) hybrid ADA313, Gene, 2019, vol. 690, p. 57. https://doi.org/10.1016/j.gene.2018.12.042

    Article  CAS  PubMed  Google Scholar 

  20. Zhang, Q., Zhang, Y., Wang, S., Hao, L., Wang, S., Xu, C., Jiang, F., and Li, T., Characterization of genome-wide microRNAs and their roles in development and biotic stress in pear, Planta, 2019, vol. 249, no. 3, p. 693. https://doi.org/10.1007/s00425-018-3027-2

    Article  CAS  PubMed  Google Scholar 

  21. Sharma, D., Tiwari, M., Lakhwani, D., Tripathi, R.D., and Trivedi, P.K., Differential expression of microRNAs by arsenate and arsenite stress in natural accessions of rice, Metallomics, 2015, vol. 7, no. 1, p. 174. https://doi.org/10.1039/c4mt00264d

    Article  CAS  PubMed  Google Scholar 

  22. Ivashchenko, A., Pyrkova, A., Niyazova, R., Alybayeva, A., and Baskakov, K., Prediction of miRNA binding sites in mRNA, Bioinformation, 2016, vol. 12, p. 237. https://doi.org/10.6026/97320630012237

    Article  Google Scholar 

  23. Garg, A. and Heinemann, U., A novel form of RNA double helix based on G·U and C·A+ wobble base pairing, RNA, 2018, vol. 24, p. 209. https://doi.org/10.1261/rna.064048.117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dai, X., Zhuang, Z., and Zhao, P., Computational analysis of miRNA targets in plants: current status and challenges, Brief. Bioinform., 2011, vol. 12, p. 115. https://doi.org/10.1093/bib/bbq065

    Article  CAS  PubMed  Google Scholar 

  25. Niyazova, R., Berillo, O., Atambayeva, Sh., Pyrkova, A., Alybayeva, A., and Ivashchenko, A., miR-1322 binding sites in paralogous and orthologous genes, Mol. Phylogenet., 2014, vol. 2015, p. 962637. https://doi.org/10.1155/2015/962637

    Article  CAS  Google Scholar 

  26. Kamenova, S.U., The characteristics of miRNA binding sites in mRNA of ZFHX3 gene and its orthologs, Vavilov J. Genet. Breed., 2018, vol. 22, p. 438. https://doi.org/10.18699/VJ18.380

    Article  Google Scholar 

  27. Yurikova, O.Yu., Aisina, D.E., Niyazova, R.E., Atambayeva, Sh.A., Labeit, S., and Ivashchenko, A.T., The interaction of miRNA-5p and miRNA-3p with the mRNAs of orthologous genes, Mol. Biol., 2019, vol. 53, p. 612. https://doi.org/10.1134/S0026893319040174

    Article  CAS  Google Scholar 

  28. Bari, A., Sagaidak, I., Pinskii, I., Orazova, S., and Ivashchenko, A., Binding of miR396 to mRNA of genes encoding growth-regulating transcription factors of plants, Russ. J. Plant Physiol., 2014, vol. 61, p. 807. https://doi.org/10.1134/S1021443714050033

    Article  CAS  Google Scholar 

  29. Bari, A., Orazova, A., and Ivashchenko, A., miR156- and miR171-binding sites in the protein-coding sequences of several plant genes, Biomed. Res. Int., 2013, vol. 2013: 307145. https://doi.org/10.1155/2013/307145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Al-Farabi Kazakh National University, Almaty, Kazakhstan

    A. K. Rakhmetullina, A. Yu. Pyrkova, A. V. Goncharova & A. T. Ivashchenko

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  1. A. K. Rakhmetullina
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  2. A. Yu. Pyrkova
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  3. A. V. Goncharova
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  4. A. T. Ivashchenko
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Correspondence to A. T. Ivashchenko.

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The present article does not contain any studies carried out with either people or animals as subjects.

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Translated by M. Bibov

Abbreviations: CDS—coding sequence; miRNA—small RNA that inhibits mRNA translation; mRNA—messenger ribonucleic acid; ∆G—free energy of miRNA binding; ΔGm—free energy of miRNA binding to a fully complementary nucleotide sequence; n.—nucleotide; TCP—the transcription factor family of plants (Teosinte branched1/Cincinnata/proliferating cell factor (TCP) family); 3'UTR—3'-untranslated region; 5'UTR—5'-untranslated region.

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Rakhmetullina, A.K., Pyrkova, A.Y., Goncharova, A.V. et al. Predicting Characteristics of the Potentially Binding Sites for miRNA in the mRNA of the TCP Transcription Factor Genes of Plants. Russ J Plant Physiol 67, 606–617 (2020). https://doi.org/10.1134/S1021443720040147

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