In silico comparative transcriptome analysis of Papaver somniferum cultivars
Tuğba Gürkök Tan
Cankiri Karatekin University, Food and Agriculture Vocational School, Department of Field Crops 18100, Cankiri, Turkeyhttps://orcid.org/0000-0003-0599-5628
Mine Türktaş
Gazi University, Department of Biology, 06100 Ankara, Turkeyhttps://orcid.org/0000-0001-8089-3774
Gülşen Güçlü
Sivas Cumhuriyet University, Health Services Vocational School, Department of Health Programmes, Sivas, Turkeyhttps://orcid.org/0000-0002-3599-213X
Abstract
Papaver somniferum is a medicinal plant of the Papaveraceae family that has traditionally been used for diet or its therapeutic value for thousands of years. Mainly, morphine and noscapine alkaloids exhibit anti-analgesic and anti-cancer effects. However, gene expression patterns and regulatory elements, such as transcription factors between different tissues, still need to be detected. In this study, comparative in silico transcriptome analyses were conducted to examine the tissue-specificity of the benzylisoquinoline alkaloids (BIAs) biosynthetic genes and transcription factors (TFs) between morphine and noscapine cultivars. Analysis showed that BIA biosynthetic genes are expressed in a different pattern between two varieties. Results showed that some members of plant-specific secondary metabolites related to TF families, such as MYB, MADS-box, bHLH, NAC, and WRKY, are differentially expressed between tissues and varieties.
Keywords:
BIA pathway genes, Papaver somniferum L., tissue specificity, transcription factors, transcriptomeReferences
Agarwal, P., Pathak, S., Lakhwani, D., Gupta, P., Asif, M.H., Trivedi, P.K. (2015). Comparative analysis of transcription factor gene families from papaver somniferum: identification of regulatory factors involved in benzylisoquinoline alkaloid biosynthesis. Protoplasma, 253(3), 857–871. https://doi.org/10.1007/s00709-015-0848-8 DOI: https://doi.org/10.1007/s00709-015-0848-8
Alagoz, Y., Gurkok, T., Zhang, B., Unver, T. (2016). Manipulating the biosynthesis of bioactive compound alkaloids for next-generation metabolic engineering in opium poppy using CRISPR-Cas 9 genome editing technology. Sci. Rep., 6(1). https://doi.org/10.1038/srep30910 DOI: https://doi.org/10.1038/srep30910
Boke, H., Ozhuner, E., Turktas, M., Parmaksiz, I., Ozcan, S., Unver, T. (2015). Regulation of the alkaloid biosynthesis by MIRNA in opium poppy. Plant Biotechnol. J., 13(3), 409–420. https://doi.org/10.1111/pbi.12346 DOI: https://doi.org/10.1111/pbi.12346
Cao, Y., Li, K., Li, Y., Zhao, X., Wang, L. (2020). MYB transcription factors as regulators of secondary metabolism in plants. Biology, 9(3), 61. https://doi.org/10.3390/biology9030061 DOI: https://doi.org/10.3390/biology9030061
Chen, S., Niu, X., Guan, Y., Li, H. (2017). Genome-wide analysis and expression profiles of the MYB genes in Brachypodium Distachyon. Plant Cell Physiol., 58(10), 1777–1788. https://doi.org/10.1093/pcp/pcx115 DOI: https://doi.org/10.1093/pcp/pcx115
Deng, X., Zhao, L., Fang, T., Xiong, Y., Ogutu, C., Yang, D., Vimolmangkang, S., Liu, Y., Han, Y. (2018). Investigation of benzylisoquinoline alkaloid biosynthetic pathway and its transcriptional regulation in Lotus. Hortic. Res., 5(1). https://doi.org/10.1038/s41438-018-0035-0 DOI: https://doi.org/10.1038/s41438-018-0035-0
Desgagné-Penix, I., Farrow, S.C., Cram, D., Nowak, J., Facchini, P.J. (2012). Integration of deep transcript and targeted metabolite profiles for eight cultivars of opium poppy. Plant Mol. Biol., 79(3), 295–313. https://doi.org/10.1007/s11103-012-9913-2 DOI: https://doi.org/10.1007/s11103-012-9913-2
Desgagné-Penix, I., Khan, M.F., Schriemer, D.C., Cram, D., Nowak, J., Facchini, P.J. (2010). Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol., 10(1). https://doi.org/10.1186/1471-2229-10-252 DOI: https://doi.org/10.1186/1471-2229-10-252
Drea Sinéad, Hileman, L.C., de Martino, G., Irish, V.F. (2007). Functional analyses of genetic pathways controlling petal specification in poppy. Development, 134(23), 4157–4166. https://doi.org/10.1242/dev.013136 DOI: https://doi.org/10.1242/dev.013136
Facchini, P.J., De Luca, V. (1994). Differential and tissue-specific expression of a gene family for tyrosine/DOPA decarboxylase in opium poppy. J. Biol. Chem., 269(43), 26684–26690. https://doi.org/10.1016/s0021-9258(18)47073-1 DOI: https://doi.org/10.1016/S0021-9258(18)47073-1
Facchini, P.J., Bird, D.A., St-Pierre, B. (2004). Can arabidopsis make complex alkaloids? Trends Plant Sci., 9(3), 116–122. https://doi.org/10.1016/j.tplants.2004.01.004 DOI: https://doi.org/10.1016/j.tplants.2004.01.004
Facchini, P.J., Hagel, J.M., Liscombe, D.K., Loukanina, N., MacLeod, B.P., Samanani, N., Zulak, K.G. (2007). Opium poppy: blueprint for an alkaloid factory. Phytochem. Rev., 6(1), 97–124. https://doi.org/10.1007/s11101-006-9042-0 DOI: https://doi.org/10.1007/s11101-006-9042-0
Farrow, S.C., Hagel, J.M., Beaudoin, G.A., Burns, D.C., Facchini, P.J. (2015). Stereochemical inversion of (s)-reticuline by a cytochrome P450 fusion in opium poppy. Nat. Chem. Biol., 11(9), 728–732. https://doi.org/10.1038/nchembio.1879 DOI: https://doi.org/10.1038/nchembio.1879
Gesell, A., Rolf, M., Ziegler, J., Díaz Chávez, M.L., Huang, F.-C., Kutchan, T.M. (2009). CYP719B1 is salutaridine synthase, the C-C phenol-coupling enzyme of morphine biosynthesis in opium poppy. J. Biol. Chem., 284(36), 24432–24442. https://doi.org/10.1074/jbc.m109.033373 DOI: https://doi.org/10.1074/jbc.M109.033373
Grothe, T., Lenz, R., Kutchan, T.M. (2001). Molecular characterization of the salutaridinol 7-O-acetyltransferase involved in morphine biosynthesis in opium poppy Papaver somniferum. J. Biol. Chem., 276(33), 30717–30723. https://doi.org/10.1074/jbc.m102688200 DOI: https://doi.org/10.1074/jbc.M102688200
Guo, L., Winzer, T., Yang, X., Li, Y., Ning, Z., He, Z., Teodor, R., Lu, Y., Bowser, T.A., Graham, I.A., Ye, K. (2018). The opium poppy genome and morphinan production. Science, 362(6412), 343–347. https://doi.org/10.1126/science.aat4096 DOI: https://doi.org/10.1126/science.aat4096
Gurkok, T., Ozhuner, E., Parmaksiz, I., Özcan, S., Turktas, M., İpek, A., Demirtas, I., Okay, S., Unver, T. (2016). Functional characterization of 4′OMT and 7OMT genes in BIA biosynthesis. Front. Plant Sci., 7. https://doi.org/10.3389/fpls.2016.00098 DOI: https://doi.org/10.3389/fpls.2016.00098
Gurkok, T., Turktas, M., Parmaksiz, I., Unver, T. (2014). Transcriptome profiling of alkaloid biosynthesis in elicitor induced opium poppy. Plant Mol. Biol. Rep., 33(3), 673–688. https://doi.org/10.1007/s11105-014-0772-7 DOI: https://doi.org/10.1007/s11105-014-0772-7
Hagel, J.M., Facchini, P.J. (2013). Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol., 54(5), 647–672. https://doi.org/10.1093/pcp/pct020 DOI: https://doi.org/10.1093/pcp/pct020
Jin, J., Tian, F., Yang, D.-C., Meng, Y.-Q., Kong, L., Luo, J., Gao, G. (2016). PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res., 45(D1). https://doi.org/10.1093/nar/gkw982 DOI: https://doi.org/10.1093/nar/gkw982
Kakeshpour, T., Nayebi, S., Rashidi Monfared, S., Moieni, A., Karimzadeh, G. (2015). Identification and expression analyses of MYB and WRKY transcription factor genes in Papaver somniferum L. Physiol. Mol. Biol. Plants, 21(4), 465–478. https://doi.org/10.1007/s12298-015-0325-z DOI: https://doi.org/10.1007/s12298-015-0325-z
Kim, D., Langmead, B., Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat. Methods, 12(4), 357–360. https://doi.org/10.1038/nmeth.3317 DOI: https://doi.org/10.1038/nmeth.3317
Li, H.-L., Wei, L.-R., Guo, D., Wang, Y., Zhu, J.-H., Chen, X.-T., Peng, S.-Q. (2016). HbMADS4, a MADS-box transcription factor from Hevea brasiliensis, negatively regulates hbsrpp. Front. Plant Sci., 7. https://doi.org/10.3389/fpls.2016.01709 DOI: https://doi.org/10.3389/fpls.2016.01709
Mishra, S., Triptahi, V., Singh, S., Phukan, U.J., Gupta, M.M., Shanker, K., Shukla, R.K. (2013). Wound induced tanscriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PSWRKY transcription factor from Papaver somniferum. PLoS ONE, 8(1). https://doi.org/10.1371/journal.pone.0052784 DOI: https://doi.org/10.1371/journal.pone.0052784
Sukumari Nath, V., Kumar Mishra, A., Kumar, A., Matoušek, J., Jakše, J. (2019). Revisiting the role of transcription factors in coordinating the defense response against citrus bark cracking viroid infection in commercial hop (Humulus lupulus L.). Viruses, 11(5), 419. https://doi.org/10.3390/v11050419 DOI: https://doi.org/10.3390/v11050419
TMO. (2017). 2016 Poppy Report. Turkish Grain Board General Directorate, Ankara.
Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L. (2010). Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol., 28(5), 511–515. https://doi.org/10.1038/nbt.1621 DOI: https://doi.org/10.1038/nbt.1621
Uimari, A., Strommer, J. (1997). Myb26: A MYB-like protein of pea flowers with affinity for promoters of phenylpropanoid genes. Plant J., 12(6), 1273–1284. https://doi.org/10.1046/j.1365-313x.1997.12061273.x DOI: https://doi.org/10.1046/j.1365-313x.1997.12061273.x
Wang, K., Li, M., Hakonarson, H. (2010). ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucl. Acids Res., 38(16). https://doi.org/10.1093/nar/gkq603 DOI: https://doi.org/10.1093/nar/gkq603
Winzer, T., Gazda, V., He, Z., Kaminski, F., Kern, M., Larson, T.R., Li, Y., Meade, F., Teodor, R., Vaistij, F.E., Walker, C., Bowser, T.A., Graham, I.A. (2012). A papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science, 336(6089), 1704–1708. https://doi.org/10.1126/science.1220757 DOI: https://doi.org/10.1126/science.1220757
Yamada, Y., Sato, F. (2013). Transcription factors in alkaloid biosynthesis. Int. Rev. Cell Mol. Biol., 339–382. https://doi.org/10.1016/b978-0-12-407695-2.00008-1 DOI: https://doi.org/10.1016/B978-0-12-407695-2.00008-1
Zhao, X., Yuan, X., Chen, S., Fu, D.-Q., Jiang, C.-Z. (2019). Metabolomic and transcriptomic analyses reveal that a MADS-box transcription factor TDR4 regulates tomato fruit quality. Front. Plant Sci., 10. https://doi.org/10.3389/fpls.2019.00792 DOI: https://doi.org/10.3389/fpls.2019.00792
Ziegler, J., Facchini, P.J., Geißler, R., Schmidt, J., Ammer, C., Kramell, R., Voigtländer, S., Gesell, A., Pienkny, S., Brandt, W. (2009). Evolution of morphine biosynthesis in opium poppy. Phytochemistry, 70(15‒16), 1696–1707. https://doi.org/10.1016/j.phytochem.2009.07.006 DOI: https://doi.org/10.1016/j.phytochem.2009.07.006
Ziegler, J., Voigtländer, S., Schmidt, J., Kramell, R., Miersch, O., Ammer, C., Gesell, A., Kutchan, T. M. (2006). Comparative transcript and alkaloid profiling inpapaverspecies identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis. The Plant Journal, 48(2), 177–192. https://doi.org/10.1111/j.1365-313x.2006.02860.x DOI: https://doi.org/10.1111/j.1365-313X.2006.02860.x
Cankiri Karatekin University, Food and Agriculture Vocational School, Department of Field Crops 18100, Cankiri, Turkey https://orcid.org/0000-0003-0599-5628
Gazi University, Department of Biology, 06100 Ankara, Turkey https://orcid.org/0000-0001-8089-3774
Sivas Cumhuriyet University, Health Services Vocational School, Department of Health Programmes, Sivas, Turkey https://orcid.org/0000-0002-3599-213X
License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.