Exploring the Effect of Methyl Jasmonate on the Expression of miR160 and miR166 and their Targeted Genes of Ajowan (Trachyspermum ammi (L.) Sprague) Medicinal Plant

Document Type : Research Paper

Authors

1 Department of Plant Production and Genetics, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran

2 Department of vegetables and irrigated pulse crop research, Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization, Karaj, Iran

Abstract

Methyl jasmonate (MeJA) is a regulator that mediates the biosynthesis of secondary metabolism compounds. Plant microRNAs (miRNAs) play important roles in post-transcriptional gene regulation of plant growth, hormone signaling, and stress response. To explore the possible role of miRNAs in regulating the MeJA signaling pathway, here we investigated the effects of MeJA treatment on the expression of candidate miRNAs and their targets in Trachyspermum ammi. The study aimed to reveal the function of miR166 and miR166 in the controlled pathway of MeJA. To achieve our goal, two MeJA levels (0 and 100 mM) were conducted at four-point times (0, 6, 12, and 24 h). The findings elucidated that pri-miR160 and pri-miR166 have increased in response to MeJA. This suggested that pri-miR160 and pri-miR166 are relevant to hormone transmission. This study suggested that monitoring microRNA expression in response to MeJA plays a significant role in T. ammi and highlights the co-expression regulatory networks on the miR160/166 target genes in coordinating growth with environmental factors. However, to better understand how the response MeJA is regulated by microRNAs, further analysis of JA pathway biosynthesis and signaling events is required.

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  1. Li P., Tian Z., Zhang Q., Zhang Y., Wang M., Fang X., Shi W., Cai X. MicroRNAome Profile of Euphorbia kansui in Response to Methyl Jasmonate. Int. J. Mol. Sci. 2019; 20(6): 1267. https://doi.org/10.3390/ijms20061267.
  2. Wang M., Wang Q., Wang B. Identification and characterization of microRNAs in Asiatic cotton (Gossypium arboreum L.). PLoS One. 2012; 7(4): e33696. https://doi.org/10.1371/journal.pone.0033696.
  3. Schluttenhofer C., Pattanaik S., Patra B., Yuan L. Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genom. 2014; 15(1): 1-20. https://doi.org/10.1186/1471-2164-15-502.
  4. Ruan J., Zhou Y., Zhou M., Yan J., Khurshid M., Weng W., Cheng J., Zhang K. Jasmonic acid signaling pathway in plants. Int. J. Mol. Sci. 2019; 20(10):2479. https://doi.org/10.3390/ijms20102479.
  5. De Geyter., N., Gholami A., Goormachtig S., Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci. 2012; 17(6): 349-59. https://doi.org/10.1016/j.tplants.2012.03.001.
  6. Wang H., Yang J.F., Deng K., He X.Y., Zhan R.T., Tang L. Methyl Jasmonate affects metabolism and gene transcription of volatile terpenoids from Amomum villosum Lour. World Sci. Technol. Mod. Tradit. Chin. Med. Mater. Med. 2014;16:1528–1536. doi: 10.11842/wst.2014.07.013.
  7. Zhang W.J., Cao X.Y., Jiang J.H. Triterpene biosynthesis in Euphorbia pekinensis induced by methyl jasmonate. Guihaia. 2015;35:590–596. doi: 10.11931/guihaia.gxzw201405011.
  8. Zhang L., Yang B., Lu B., Kai G., Wang Z., Xia Y., Ding R., Zhang H., Sun X., Chen W. Tropane alkaloids production in transgenic Hyoscyamus niger hairy root cultures over-expressing putrescinen-methyltransferase is methyl jasmonate-dependent. Planta. 2007;225:887–896. doi: 10.1007/s00425-006-0402-1.
  9. Sunkar R., Li Y.-F., Jagadeeswaran G. Functions of microRNAs in plant stress responses. Trends Plant Sci. 2012;17:196–203. doi: 10.1016/j.tplants.2012.01.010.
  10. Kajal M., Singh K. Small RNA profiling for identification of miRNAs involved in regulation of saponins biosynthesis in Chlorophytum borivilianum. BMC Plant Biol. 2017; 17: 265.
  11. Li X., Xie X., Li J., Cui Y., Hou Y., Zhai L., Wang X., Fu Y., Liu R., Bian S. Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol. 2017; 17(1): 1-18. https://doi.org/10.1186/s12870-017-0983-9.
  12. Shen E.M., Singh S.K.; Ghosh J.S.; Patra B.; Paul P.; Yuan L.; Pattanaik S. The miRNAome of Catharanthus roseus: identification, expression analysis, and potential roles of microRNAs in regulation of terpenoid indole alkaloid biosynthesis. Sci. Rep. 2017; 7: 43027;
  13. Qiu D., Pan X., Wilson I.W., Li F., Liu M., Teng W., Zhang B. High throughput sequencing technology reveals that the taxoid elicitor methyl jasmonate regulates microRNA expression in Chinese yew (Taxus chinensis) Gene. 2009;436:37–44. doi: 10.1016/j.gene.2009.01.006.
  14. Xu S., Jiang Y.M., Wang N., Xia B., Jiang Y.L., Li X.D., Zhang Z.Z., Li Y.K., Wang R. Identification and differential regulation of microRNAs in response to methyl jasmonate treatment in Lycoris aurea by deep sequencing. BMC Genom. 2016;17:789–803. doi: 10.1186/s12864-016-2645-y.
  15. Amiripour M., Sadat Noori S.A., Shariati V., Soltani Howyzeh M. Transcriptome analysis of Ajowan (Trachyspermum ammi L.) inflorescence. J. Plant Biochem. Biotechnol. 2019; 28: 496-508.
  16. Hanif M.A., Hassan S.M., Mughal S.S., Rehman A.; Hassan S.K., Ibrahim A., Hassan H. An overview on ajwain (Trachyspermum Ammi) pharmacological effects: current and conventional. Technol. 2021; 5(1): 1-6.
  17. Davazdahemami S., Allahdadi M. Essential oil yield and composition of four annual plants (ajowan, dill, Moldavian balm and black cumin) under saline irrigation. Food Ther. Health Care. 2022, 4(5)..
  18. Shams S., Ismaili A., Firouzabadi F.N., Mumivand H., Sorkheh K. Comparative transcriptome analysis to identify putative genes involved in carvacrol biosynthesis pathway in two species of Satureja, endemic medicinal herbs of Iran. Plos one. 2023; 18(7): 0281351.
  19. Ncube B., Van Staden J. Tilting plant metabolism for improved metabolite biosynthesis and enhanced human benefit. Molecules. 2015; 20(7): 12698-12731.
  20. Kaur J., Singh A., Pathak T., Kumar K. Role of PGRs in anticancer alkaloids (Vincristine and Vinblastine) production. Catharanthus roseus. Springer, Cham. 2017; pp 309–319.
  21. Soltani Howyzeh M., Sadat Noori S.A., Shariati J, V., Amiripour, M. Comparative transcriptome analysis to identify putative genes involved in thymol biosynthesis pathway in medicinal plant Trachyspermum ammi L. Sci. Rep. 2018; 8(1): 13405.
  22. Varkonyi-Gasic E., Wu R., Wood M. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007, 3(1), 1-2.
  23. Warde-Farley D., Donaldson S.L., Comes O., Zuberi K., Badrawi R., Chao P., Franz M., Grouios, C., Kazi, F., Lopes, C.T., Maitland, A. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 2010; 38(suppl_2): W214-W220.
  24. Kieffer M., Stern Y., Cook H., Clerici E., Maulbetsch C., Laux T., Davies B. Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. The Plant Cell. 2006; 18(3): 560-573.
  25. Ding Y., Tao Y., Zhu C. Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 2013; 64; 3077–3086. https://doi: 10.1093/jxb/ert164
  26. Liu P.P., Montgomery T.A., Fahlgren N., Kasschau K.D., Nonogaki H., Carrington J.C. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post‐germination stages. Plant J. 2007; 52(1): 133-46.
  27. Dai X., Lu Q., Wang J., Wang L., Xiang F., Liu Z. MiR160 and its target genes ARF10, ARF16 and ARF17 modulate hypocotyl elongation in a light, BRZ, or PAC-dependent manner in Arabidopsis: miR160 promotes hypocotyl elongation. Plant Sci. 2021; 303: 110686.
  28. Zhang F., Yang J., Zhang N., Wu J., Si H. Roles of microRNAs in abiotic stress response and characteristics regulation of plant. Front. Plant Sci. 2022; 13: 919243.
  29. Mallory A.C., Bartel D.P., Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell. 2005; 17(5): 1360-1375.
  30. Chavez Montes, R.A., Rosas-Cárdenas, D.F.F., De Paoli, E., Accerbi, M., Rymarquis, L.A., Mahalingam G., Marsch-Martínez N., Meyers B.C., Green P.J., De Folter S. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat. Commun. 2014; 5(1): 1-15.
  31. Gutierrez L., Mongelard G., Flokova K., Pacurar D. I., Novak O., Staswick P., Păcurar M., Demailly H., Geiss G., Bellini C. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell. 2012; 24: 2515–2527.
  32. Wilkinson S.W., Vivian-Smith A., Krokene P., Mageroy M.H. The microRNA response associated with methyl jasmonate-induced resistance in Norway spruce bark. Plant Gene. 2021; 27: 100301.
  33. Mageroy M.H., Wilkinson S.W., Tengs T., Cross H., Almvik M., Pétriacq P., Vivian‐Smith, A., Zhao T.; Fossdal C.G., Krokene P. Molecular underpinnings of methyl jasmonate‐induced resistance in Norway spruce. Plant Cell Environ. 2020; 43(8): 1827-1843.
  34. Guo Z., Hao K., Lv Z., Yu L., Bu Q., Ren J., Zhang H., Chen R., Zhang L. Profiling of phytohormone-specific microRNAs and characterization of the miR160-ARF1 module involved in glandular trichome development and artemisinin biosynthesis in Artemisia annua. Plant Biotechnol J. 2023;21(3):591-605.
  35. Axtell M.J., Snyder J.A., Bartel D.P. Common functions for diverse small RNAs of land plants. Plant J. 2007; 19(6): 1750-1769.
  36. Roy S., Chakraborty A.P., Chakraborty R. Understanding the potential of root microbiome influencing salt‐tolerance in plants and mechanisms involved at the transcriptional and translational level. Physiol. Plant. 2021; 173(4): 1657-1681.