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Computational Identification of Citrus reticulata L. microRNAs and the Cis-Acting Regulatory Elements to Predict the Expression Probability of Their Respective MIR Genes

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Abstract

MicroRNA(miRNA), a small non-coding class of RNA that regulates the gene expression, is conserved among several plant species. In the present study, an in-silico approach was adopted to identify miRNA from the known expressed sequence tags (ESTs) of Citrus reticulata L. A total of 17 miRNAs from 23 different ESTs along with their secondary structures and targets were predicted. The identified 63 targets include several transcription factors, proteins that regulate plant growth, development, flowering, and seed development together with stress response. The cis-regulatory element present at the promoter region of the MIR genes of C. reticulata describes their role during light responsiveness, auxin, gibberellins, abscisic acid (ABA), anthocyanin responsiveness, salicylic acid responsiveness, anaerobic induction, circadian control, nitrate dependent regulation of the cell cycle and DNA replication, defense, and stress responsiveness. The present study identifies the miRNAs along with their regulatory elements in C. reticulata. The study will also be useful for the research on identification from the genomic data of different plants and prediction of expression probability of identified MIR genes based on the presence of upstream promoter and other regulatory elements.

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REFERENCES

  1. Baghban Kohnehrouz, B., Bastami, M., and Nayeri, S., In silico identification of novel microRNAs and targets using EST analysis in Allium cepa L., Interdiscip. Sci.: Comput. Life Sci., 2018, vol. 10, pp. 771–780.

    Article  CAS  Google Scholar 

  2. Barrett, H. and Rhodes, A., A numerical taxonomic study of affinity relationships in cultivated Citrus and its close relatives, Syst. Bot., 1976, pp. 105–136.

  3. Baumberger, N. and Baulcombe, D., Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs, Proc. Natl. Acad. Sci., 2005, vol. 102, pp. 11928–11933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bologna, N.G., Schapire, A.L., Zhai, J., Chorostecki, U., Boisbouvier, J., Meyers, B.C., and Palatnik, J.F., Multiple RNA recognition patterns during microRNA biogenesis in plants, Genome Res., 2013, vol. 23, pp. 1675–1689.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bravo, L., Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance, Nutr. Rev., 1998, vol. 56, pp. 317–333.

    Article  CAS  PubMed  Google Scholar 

  6. Brivanlou, A.H. and Darnell, Jr.J.E., Signal transduction and the control of gene expression, Science, 2002, vol. 295, pp. 813–818.

    Article  CAS  PubMed  Google Scholar 

  7. Chen, X., Li, Q., Wang, J., Guo, X., Jiang, X., Ren, Z., Weng, C., Sun, G., Wang, X., and Liu, Y., Identification and characterization of novel amphioxus microRNAs by Solexa sequencing, Genome Biol., 2009, vol. 10, pp. 1–13.

    Article  Google Scholar 

  8. Chowdhury, M.R., Basak, J., and Bahadur, R.P., Elucidating the functional role of predicted miRNAs in post-transcriptional gene regulation along with Symbiosis in Medicago truncatula, Curr. Bioinf., 2020, vol. 15, pp. 108–120.

    Article  CAS  Google Scholar 

  9. Consortium, G.O., Gene ontology consortium: going forward, Nucleic Acids Res., 2015, vol. 43, pp. D1049–D1056.

    Article  Google Scholar 

  10. Devi, K.J., Chakraborty, S., Deb, B., and Rajwanshi, R., Computational identification and functional annotation of microRNAs and their targets from expressed sequence tags (ESTs) and genome survey sequences (GSSs) of coffee (Coffea arabica L.), Plant Gene, 2016, vol. 6, pp. 30–42.

    Article  CAS  Google Scholar 

  11. Dezulian, T., Remmert, M., Palatnik, J.F., Weigel, D., and Huson, D.H., Identification of plant microRNA homologs, Bioinformatics, 2006, vol. 22, pp. 359–360.

    Article  CAS  PubMed  Google Scholar 

  12. Ding, Y., Chen, Z., and Zhu, C., Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa), J. Exp. Bot., 2011, vol. 62, pp. 3563–3573.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Elhiti, M. and Stasolla, C., Structure and function of homodomain-leucine zipper (HD-Zip) proteins, Plant Signaling Behav., 2009, vol. 4, pp. 86–88.

    Article  CAS  Google Scholar 

  14. Fan, F., Yang, X., Cheng, Y., Kang, Y., and Chai, X., The DnaJ gene family in pepper (Capsicum annuum L.): comprehensive identification, characterization and expression profiles, Front. Plant Sci., 2017, vol. 8, p. 689.

    Article  PubMed  PubMed Central  Google Scholar 

  15. FAO (2019). Citrus Fruit Fresh and Processed Statistical Bulletin 2020. https://www.fao.org/3/cb6492en/ b6492en.pdf. Accessed May 16, 2023.

  16. Frazier, T.P., Xie, F., Freistaedter, A., Burklew, C.E., and Zhang, B., Identification and characterization of microRNAs and their target genes in tobacco (Nicotiana tabacum), Planta, 2010, vol. 232, pp. 1289–1308.

    Article  CAS  PubMed  Google Scholar 

  17. Gbaj, M.A., Sadawe, I.A., Meiqal, N.M., Bensaber, S.M., Maamar, M.S., Hermann, A., and Gbaj, A.M., Evaluation of neuropharmacological activities of methanolic and aqueous extracts of Citrus reticulata (Rutaceae) fruit peels, Am. J. Biomed. Sci. Res., 2019, vol. 2, pp. 131–135.

    Article  Google Scholar 

  18. Griffiths-Jones, S., Grocock, R.J., Van Dongen, S., Bateman, A., and Enright, A.J., miRBase: microRNA sequences, targets and gene nomenclature, Nucleic Acids Res., 2006, vol. 34, pp. D140–D144.

    Article  CAS  PubMed  Google Scholar 

  19. Griffiths-Jones, S., Saini, H.K., van Dongen, S., and Enright, A.J., miRBase: tools for microRNA genomics, Nucleic Acids Res., 2007, vol. 36, pp. D154–D158.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hall, T., Biosciences, I., and Carlsbad, C., BioEdit: an important software for molecular biology, GERF Bull Biosci., 2011, vol. 2, pp. 60–61.

    Google Scholar 

  21. Han, Y.-Q., Hu, Z., Zheng, D.-F., and Gao, Y.M., Analysis of promoters of microRNAs from a Glycine max degradome library, J. Zhejiang Univ., Sci., B., 2014, vol. 15, pp. 125–132.

    Article  CAS  PubMed  Google Scholar 

  22. Hao, X., Wang, B., Wang, L., Zeng, J., Yang, Y., and Wang, X., Comprehensive transcriptome analysis reveals common and specific genes and pathways involved in cold acclimation and cold stress in tea plant leaves, Sci. Hortic., 2018, vol. 240, pp. 354–368.

    Article  CAS  Google Scholar 

  23. Hassan, A.Z., Ahmed, K.M., Abu-Gabal, N.S., Mahrous, K.F., and Shalaby, N.M., Phytochemical and genotoxicity studies of Citrus reticulata aerial part in mice, Egypt. Pharm. J., 2017, vol. 16, p. 87.

    Article  Google Scholar 

  24. Hindi, N.K.K. and Chabuck, Z.A.G., Antimicrobial activity of different aqueous lemon extracts, J. Appl. Pharm. Sci., 2013, vol. 3, pp. 074–078.

  25. Jagadeeswaran, G., Zheng, Y., Li, Y.F., Shukla, L.I., Matts, J., Hoyt, P., Macmil, S.L., Wiley, G.B., Roe, B.A., and Zhang, W., Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families, New Phytol., 2009, vol. 184, pp. 85–98.

    Article  CAS  PubMed  Google Scholar 

  26. Jones-Rhoades, M.W., Bartel, D.P., and Bartel, B., MicroRNAs and their regulatory roles in plants, Annu. Rev. Plant Biol., 2006, vol. 57, pp. 19–53.

    Article  CAS  PubMed  Google Scholar 

  27. Kangralkar, V., Gavimath, C., Vijapur, V., Gowri, B., Hooli, V., and Mathapati, P., Protective effect of essential oil of Citrus reticulata on isoniazid induced hepatotoxicity in Wistar rats, Int. J. Pharm. Appl., 2010, vol. 1.

  28. Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 1980, vol. 16, pp. 111–120.

    Article  CAS  PubMed  Google Scholar 

  29. Kong, F., Deng, Y., Zhou, B., Wang, G., Wang, Y., and Meng, Q., A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress, J. Exp. Bot., 2014, vol. 65, pp. 143–158.

    Article  CAS  PubMed  Google Scholar 

  30. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., MEGA X: molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, pp. 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lin, Y. and Lai, Z., Comparative analysis reveals dynamic changes in miRNAs and their targets and expression during somatic embryogenesis in longan (Dimocarpus longan Lour.), PLoS One, 2013, vol. 8, p. e60337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Liu, Y., Heying, E., and Tanumihardjo, S.A., History, global distribution, and nutritional importance of citrus fruits, Compr. Rev. Food Sci. Food Saf., 2012, vol. 11, pp. 530–545.

    Article  CAS  Google Scholar 

  33. Lu, Y.-B., Qi, Y.-P., Yang, L.-T., Guo, P., Li, Y., and Chen, L.-S., Boron-deficiency-responsive microRNAs and their targets in Citrus sinensis leaves, BMC Plant Biol., 2015, vol. 15, pp. 1–15.

    Article  Google Scholar 

  34. Ma, C.-L., Qi, Y.-P., Liang, W.-W., Yang, L.-T., Lu, Y.-B., Guo, P., Ye, X., and Chen, L.-S., MicroRNA regulatory mechanisms on Citrus sinensis leaves to magnesium-deficiency, Front. Plant Sci., 2016, vol. 7, p. 201.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Mallory, A.C. andVaucheret, H., Functions of microRNAs and related small RNAs in plants, Nat. Genet., 2006, vol. 38, p. S31.

    Article  CAS  PubMed  Google Scholar 

  36. Megraw, M., Baev, V., Rusinov, V., Jensen, S.T., Kalantidis, K., and Hatzigeorgiou, A.G., MicroRNA promoter element discovery in Arabidopsis, RNA, 2006, vol. 12, pp. 1612–1619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Mishra, A.K., Duraisamy, G.S., Týcová, A., and Matoušek, J., Computational exploration of microRNAs from expressed sequence tags of Humulus lupulus, target predictions and expression analysis, Comput. Biol. Chem., 2015, vol. 59, pp. 131–141.

    Article  CAS  PubMed  Google Scholar 

  38. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A.C., and Kanehisa, M., KAAS: an automatic genome annotation and pathway reconstruction server, Nucleic Acids Res., 2007, vol. 35, pp. W182–W185.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Motameny, S., Wolters, S., Nürnberg, P., and Schumacher, B., Next generation sequencing of miRNAs–strategies, resources and methods, Genes, 2010, vol. 1, pp. 70–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pandey, B., Gupta, O.P., Pandey, D.M., Sharma, I., and Sharma, P., Identification of new stress-induced microRNA and their targets in wheat using computational approach, Plant Signaling Behav., 2013, vol. 8, p. e23932.

    Article  Google Scholar 

  41. Qiu, X.-B., Shao, Y.-M., Miao, S., and Wang, L., The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones, Cell. Mol. Life Sci. CMLS, 2006, vol. 63, pp. 2560–2570.

    Article  CAS  PubMed  Google Scholar 

  42. Rajwanshi, R., Chakraborty, S., Jayanandi, K., Deb, B., and Lightfoot, D.A., Orthologous plant microRNAs: microregulators with great potential for improving stress tolerance in plants, Theor. Appl. Genet., 2014, vol. 127, pp. 2525–2543.

    Article  CAS  PubMed  Google Scholar 

  43. Ravichandran, S., Ragupathy, R., Edwards, T., Domaratzki, M., and Cloutier, S., MicroRNA-guided regulation of heat stress response in wheat, BMC Genomics, 2019, vol. 20, pp. 1–16.

    Article  CAS  Google Scholar 

  44. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P., MicroRNAs in plants, Genes Dev., 2002, vol. 16, pp. 1616–1626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rhoades, M.W., Reinhart, B.J., Lim, L.P., Burge, C.B., Bartel, B., and Bartel, D.P., Prediction of plant microRNA targets, Cell, 2002, vol. 110, pp. 513–520.

    Article  CAS  PubMed  Google Scholar 

  46. Rogers, K. and Chen, X., Biogenesis, turnover, and mode of action of plant microRNAs, Plant Cell, 2013, vol. 25, pp. 2383–2399.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rombauts, S., Déhais, P., Van Montagu, M., and Rouzé, P., PlantCARE, a plant cis-acting regulatory element database, Nucleic Acids Res., 1999, vol. 27, pp. 295–296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Shikata, M., Matsuda, Y., Ando, K., Nishii, A., Takemura, M., Yokota, A., and Kohchi, T., Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family, J. Exp. Bot., 2004, vol. 55, pp. 631–639.

    Article  CAS  PubMed  Google Scholar 

  49. Singh, A., Singh, S., Panigrahi, K.C., Reski, R., and Sarkar, A.K., Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana, Plant Cell Rep., 2014, vol. 33, pp. 945–953.

    Article  CAS  PubMed  Google Scholar 

  50. Singh, R., Tiwari, J.K., Rawat, S., Sharma, V., and Singh, B.P., In silico identification of candidate microRNAs and their targets in potato somatic hybrid Solanum tuberosum (+) S. pinnatisectum for late blight resistance, Plant Omics, 2016, vol. 9, pp. 159–164.

    Article  Google Scholar 

  51. Solovyev, V.V., Shahmuradov, I.A., and Salamov, A.A., Identification of promoter regions and regulatory sites, in Computational Biology of Transcription Factor Binding, 2010, pp. 57–83.

  52. Song, C., Fang, J., Li, X., Liu, H., and Chao, C.T., Identification and characterization of 27 conserved microRNAs in citrus, Planta, 2009, vol. 230, pp. 671–685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Stark, A., Bushati, N., Jan, C.H., Kheradpour, P., Hodges, E., Brennecke, J., Bartel, D.P., Cohen, S.M., and Kellis, M., A single Hox locus in Drosophila produces functional microRNAs from opposite DNA strands, Genes Dev., 2008, vol. 22, pp. 8–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sultana, H.S., Ali, M., and Panda, B.P., Influence of volatile constituents of fruit peels of Citrus reticulata Blanco on clinically isolated pathogenic microorganisms under in vitro, Asian Pac. J. Trop. Biomed., 2012, vol. 2, pp. S1299–S1302.

    Article  Google Scholar 

  55. Tatematsu, K., Nakabayashi, K., Kamiya, Y., and Nambara, E., Transcription factor AtTCP14 regulates embryonic growth potential during seed germination in Arabidopsis thaliana, Plant J., 2008, vol. 53, pp. 42–52.

    Article  CAS  PubMed  Google Scholar 

  56. Tumbas, V.T., Ćetković, G.S., Đilas, S.M., Čanadanović-Brunet, J.M., Vulić, J.J., Knez, Ž., and Škerget, M., Antioxidant activity of mandarin (Citrus reticulata) peel, Acta Period. Technol., 2010, pp. 195–203.

  57. Viveka, A. and Moossab, F., Identification of novel micro RNAs and their targets in Cocos nucifera–A Bioinformatics approach, Biosci. Biotechnol. Res. Commun., 2016, vol. 9, pp. 481–488.

    Article  Google Scholar 

  58. Wang, T., Chen, L., Zhao, M., Tian, Q., and Zhang, W.-H., Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing, BMC Genomics, 2011, vol. 12, pp. 1–11.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wang, J., Chen, Z., Zhang, Q., Meng, S., and Wei, C., The NAC transcription factors OsNAC20 and OsNAC26 regulate starch and storage protein synthesis, Plant Physiol., 2020, vol. 184, pp. 1775–1791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Xia, Z., Zhang, X., Li, J., Su, X., and Liu, J., Overexpression of a tobacco J-domain protein enhances drought tolerance in transgenic Arabidopsis, Plant Physiol. Biochem., 2014, vol. 83, pp. 100–106.

    Article  CAS  PubMed  Google Scholar 

  61. Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S.A., and Carrington, J.C., Expression of Arabidopsis MIRNA genes, Plant Physiol., 2005, vol. 138, pp. 2145–2154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Xie, F., Frazier, T.P., and Zhang, B., Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum), Planta, 2010, vol. 232, pp. 417–434.

    Article  CAS  PubMed  Google Scholar 

  63. Yang, C., Liu, T., Bai, F., Wang, N., Pan, Z., Yan, X., and Peng, S., miRNAome analysis associated with anatomic and transcriptomic investigations reveal the polar exhibition of corky split vein in boron deficient Citrus sinensis, Mol. Genet. Genomics, 2015, vol. 290, pp. 1639–1657.

    Article  CAS  PubMed  Google Scholar 

  64. Yu, B., Bi, L., Zheng, B., Ji, L., Chevalier, D., Agarwal, M., Ramachandran, V., Li, W., Lagrange, T., and Walker, J.C., The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis, Proc. Natl. Acad. Sci., 2008, vol. 105, pp. 10073–10078.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhang, W., Ruan, J., Ho, T.-hD., You, Y., Yu, T., and Quatrano, R.S., Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid-and abiotic stress-responsive genes in Arabidopsis thaliana, Bioinformatics, 2005, vol. 21, pp. 3074–3081.

    Article  CAS  PubMed  Google Scholar 

  66. Zhang, B., Pan, X., Cannon, C.H., Cobb, G.P., and Anderson, T.A., Conservation and divergence of plant microRNA genes, Plant J., 2006, vol. 46, pp. 243–259.

    Article  CAS  PubMed  Google Scholar 

  67. Zhang, W., Luo, Y., Gong, X., Zeng, W., and Li, S., Computational identification of 48 potato microRNAs and their targets, Comput. Biol. Chem., 2009, vol. 33, pp. 84–93.

    Article  CAS  PubMed  Google Scholar 

  68. Zhang, Y., Zhu, X., Chen, X., Song, C., Zou, Z., Wang, Y., Wang, M., Fang, W., and Li, X., Identification and characterization of cold-responsive microRNAs in tea plant (Camellia sinensis) and their targets using high-throughput sequencing and degradome analysis, BMC Plant Biol., 2014, vol. 14, pp. 1–18.

    Article  Google Scholar 

  69. Zhang, C., Zhang, B., Ma, R., Yu, M., Guo, S., and Guo, L., Isolation and expression analysis of four HD-ZIP III family genes targeted by microRNA166 in peach, GMR, Genet. Mol. Res., 2015, vol. 14, pp. 14151–14161.

    Article  CAS  PubMed  Google Scholar 

  70. Zhu, Q.-H., Fan, L., Liu, Y., Xu, H., Llewellyn, D., and Wilson, I., miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton, PLoS One, 2013, vol. 8, pp. e84390.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Zuker, M., Mfold web server for nucleic acid folding and hybridization prediction, Nucleic Acids Res., 2003, vol. 31, pp. 3406–3415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

RR and HDC acknowledge Assam University, Silchar, Assam, India for providing infrastructural facilities to carry out the present study. The authors acknowledge the funding from Science and Engineering Research Board (SERB), Government of India vide grant no. EEQ/2016/000501.

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  1. Department of Biotechnology, Assam University Silchar, India

    Himanish Dutta Choudhury & Ravi Rajwanshi

  2. Discipline of Life Sciences, School of Sciences, Indira Gandhi National Open University, New Delhi, India

    Ravi Rajwanshi

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Choudhury, H.D., Rajwanshi, R. Computational Identification of Citrus reticulata L. microRNAs and the Cis-Acting Regulatory Elements to Predict the Expression Probability of Their Respective MIR Genes. Cytol. Genet. 57, 466–490 (2023). https://doi.org/10.3103/S009545272305002X

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