Terpenoid Biosynthetic Pathway in Ferula persica Using Transcriptome Analysis and Metabolome Data

Document Type : Original Research

Authors
1 Nuclear Agriculture Research School, Nuclear Science and Technology Research Institute, AEOI, P. O. Box: 31485-498, Karaj, Islamic Republic of Iran.
2 Department of Agronomy and Plant Breeding, Agricultural and Natural Resources College, University of Tehran, Karaj, Islamic Republic of Iran.
3 Department of Biotechnology, College of Agriculture, Isfahan University of Technology, Isfahan 84156-83111, Islamic Republic of Iran.
4 Plant Sciences Group, Wageningen University, Wageningen, The Netherlands.
Abstract
An effort was made to analyze metabolome and transcriptome profiles of Ferula persica via GC-MS and RNA-seq data. The analysis of the essential oils extracted from both flower and root tissues demonstrated the prominence of monoterpene constituents, while sesquiterpene compounds were present in the lower magnitudes. Considering transcriptome analysis, 2127 differentially expressed genes were found between root and flower: 396 transcripts were up-regulated in root, while 1731 exhibited an up-regulation pattern in flower. Out of 2127 transcripts, 86 were annotated as Terpene Synthases (TPSs), of which 83 TPSs were classified subsequently into five individual sub-families of TPS-a (33), TPS-b (42), TPS-c (2), TPSe-f (3), and TPS-g (3). Several transcription factor families were recognized among the differentially expressed genes, suggesting their direct or indirect regulatory roles for the biosynthesis of terpenoids in F. persica. Finally, according to our phylogenetic results, both F. assa-foetida and F. gummosa were placed in the same clade, while F. persica was lonely settled in one monophyletic clade, with the estimated divergence time of 2.99 Million Years Ago (MYA) between F. gummosa and F. assa-foetida, and 3.87 MYA between F. persica and two other Ferula species.

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[1] D. J. Mabberley, Mabberley's Plant-book: A Portable Dictionary of Plants, their Classification and Uses, 4 ed. Cambridge: Cambridge University Press, 2017.
[2] J. Asili, A. Sahebkar, B. S. Fazly Bazzaz, S. Sharifi, and M. Iranshahi, "Identification of Essential Oil Components of Ferula badrakema Fruits by GC-MS and 13 C-NMR Methods and Evaluation of its Antimicrobial Activity," Journal of Essential Oil Bearing Plants, vol. 12, pp. 7-15, 01/01 2009.
[3] G. Kavoosi and V. Rowshan, "Chemical composition, antioxidant and antimicrobial activities of essential oil obtained from Ferula assa-foetida oleo-gum-resin: effect of collection time," Food chemistry, vol. 138, pp. 2180-2187, 2013.
[4] A. Barzegar, M. A. Salim, P. Badr, A. Khosravi, S. Hemmati, H. Seradj, et al., "Persian asafoetida vs. sagapenum: challenges and opportunities," Research Journal of Pharmacognosy, vol. 7, pp. 71-80, 2020.
[5] J. Nasiri, E. Motamedi, M. R. Naghavi, and M. Ghafoori, "Removal of crystal violet from water using β-cyclodextrin functionalized biogenic zero-valent iron nanoadsorbents synthesized via aqueous root extracts of Ferula persica," Journal of hazardous materials, vol. 367, pp. 325-338, 2019.
[6] J. Nasiri, M. Rahimi, Z. Hamezadeh, E. Motamedi, and M. R. Naghavi, "Fulfillment of green chemistry for synthesis of silver nanoparticles using root and leaf extracts of Ferula persica: Solid-state route vs. solution-phase method," Journal of Cleaner Production, vol. 192, pp. 514-530, 2018.
[7] A. S. Najafabadi, M. R. Naghavi, H. Farahmand, and A. Abbasi, "Transcriptome and metabolome analysis of Ferula gummosa Boiss. to reveal major biosynthetic pathways of galbanum compounds," Functional & integrative genomics, vol. 17, pp. 725-737, 2017.
[8] H. Amini, M. R. Naghavi, T. Shen, Y. Wang, J. Nasiri, I. A. Khan, et al., "Tissue-specific transcriptome analysis reveals candidate genes for terpenoid and phenylpropanoid metabolism in the medicinal plant Ferula assafoetida," G3: Genes, Genomes, Genetics, vol. 9, pp. 807-816, 2019.
[9] A. M. Bolger, M. Lohse, and B. Usadel, "Trimmomatic: a flexible trimmer for Illumina sequence data," Bioinformatics, vol. 30, pp. 2114-2120, 2014.
[10] M. G. Grabherr, B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, et al., "Full-length transcriptome assembly from RNA-Seq data without a reference genome," Nature biotechnology, vol. 29, p. 644, 2011.
[11] F. A. Simão, R. M. Waterhouse, P. Ioannidis, E. V. Kriventseva, and E. M. Zdobnov, "BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs," Bioinformatics, vol. 31, pp. 3210-3212, 2015.
[12] B. Li and C. N. Dewey, "RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome," BMC bioinformatics, vol. 12, p. 323, 2011.
[13] V. Jimenez-Jacinto, A. Sanchez-Flores, and L. Vega-Alvarado, "Integrative Differential Expression Analysis for Multiple EXperiments (IDEAMEX): A Web server tool for integrated RNA-seq data analysis," Frontiers in genetics, vol. 10, p. 279, 2019.
[14] M. I. Love, W. Huber, and S. Anders, "Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2," Genome biology, vol. 15, p. 550, 2014.
[15] M. D. Robinson, D. J. McCarthy, and G. K. Smyth, "edgeR: a Bioconductor package for differential expression analysis of digital gene expression data," Bioinformatics, vol. 26, pp. 139-140, 2010.
[16] S. Tarazona, F. García, A. Ferrer, J. Dopazo, and A. Conesa, "NOIseq: a RNA-seq differential expression method robust for sequencing depth biases," EMBnet. journal, vol. 17, pp. 18-19, 2011.
[17] M. E. Ritchie, B. Phipson, D. Wu, Y. Hu, C. W. Law, W. Shi, et al., "limma powers differential expression analyses for RNA-sequencing and microarray studies," Nucleic acids research, vol. 43, pp. e47-e47, 2015.
[18] P. Priya, A. Yadav, J. Chand, and G. Yadav, "Terzyme: a tool for identification and analysis of the plant terpenome," Plant methods, vol. 14, pp. 4-4, 2018.
[19] T. Tian, Y. Liu, H. Yan, Q. You, X. Yi, Z. Du, et al., "AgriGO v2.0: A GO analysis toolkit for the agricultural community, 2017 update," Nucleic acids research, vol. 45, 05/04 2017.
[20] D. M. Emms and S. Kelly, "OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy," Genome biology, vol. 16, p. 157, 2015.
[21] M. Iorizzo, S. Ellison, D. Senalik, P. Zeng, P. Satapoomin, J. Huang, et al., "A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution," Nature Genetics, vol. 48, pp. 657-666, 2016/06/01 2016.
[22] S. Capella-Gutiérrez, J. M. Silla-Martínez, and T. Gabaldón, "trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses," Bioinformatics, vol. 25, pp. 1972-1973, 2009.
[23] A. Soorni, T. Borna, A. Alemardan, M. Chakrabarti, A. G. Hunt, and A. Bombarely, "Transcriptome landscape variation in the genus Thymus," Genes, vol. 10, p. 620, 2019.
[24] K. J. Livak and T. D. Schmittgen, "Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method," methods, vol. 25, pp. 402-408, 2001.
[25] K. Javidnia, R. Miri, M. Kamalinejad, and N. Edraki, "Chemical composition of Ferula persica Wild. essential oil from Iran," Flavour and fragrance journal, vol. 20, pp. 605-606, 2005.
[26] M. Iranshahi, G. Amin, M. S. Sourmaghi, A. Shafiee, and A. Hadjiakhoondi, "Sulphur‐containing compounds in the essential oil of the root of Ferula persica Willd. var. persica," Flavour and fragrance journal, vol. 21, pp. 260-261, 2006.
[27] Y. Yamada and F. Sato, "Transcription factors in alkaloid biosynthesis," in International review of cell and molecular biology. vol. 305, ed: Elsevier, 2013, pp. 339-382.
[28] S. Wang and M. Gribskov, "Comprehensive evaluation of de novo transcriptome assembly programs and their effects on differential gene expression analysis," Bioinformatics, vol. 33, pp. 327-333, 2017.
[29] M. Ashour, M. Wink, and J. Gershenzon, "Biochemistry of terpenoids: monoterpenes, sesquiterpenes and diterpenes," Annual Plant Reviews online, pp. 258-303, 2018.
[30] B. Singh and R. A. Sharma, "Plant terpenes: defense responses, phylogenetic analysis, regulation and clinical applications," 3 Biotech, vol. 5, pp. 129-151, 2015.
[31] G.-J. Hong, X.-Y. Xue, Y.-B. Mao, L.-J. Wang, and X.-Y. Chen, "Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression," The Plant Cell, vol. 24, pp. 2635-2648, 2012.
[32] M. M. B. Zvi, E. Shklarman, T. Masci, H. Kalev, T. Debener, S. Shafir, et al., "PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers," New Phytologist, vol. 195, pp. 335-345, 2012.
[33] Y. Ji, J. Xiao, Y. Shen, D. Ma, Z. Li, G. Pu, et al., "Cloning and characterization of AabHLH1, a bHLH transcription factor that positively regulates artemisinin biosynthesis in Artemisia annua," Plant and Cell Physiology, vol. 55, pp. 1592-1604, 2014.
[34] E. A. Spyropoulou, M. A. Haring, and R. C. Schuurink, "RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters," BMC genomics, vol. 15, p. 402, 2014.
[35] Y.-H. Xu, J.-W. Wang, S. Wang, J.-Y. Wang, and X.-Y. Chen, "Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A," Plant Physiology, vol. 135, pp. 507-515, 2004.
[36] N. Yokotani, Y. Sato, S. Tanabe, T. Chujo, T. Shimizu, K. Okada, et al., "WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance," Journal of experimental botany, vol. 64, pp. 5085-5097, 2013.
[37] M. Zhang, X. Jin, Y. Chen, M. Wei, W. Liao, S. Zhao, et al., "TcMYC2a, a basic helix–loop–helix transcription factor, transduces JA-signals and regulates taxol biosynthesis in Taxus chinensis," Frontiers in plant science, vol. 9, p. 863, 2018.
[38] K. Yoshida, N. Oyama-Okubo, and M. Yamagishi, "An R2R3-MYB transcription factor ODORANT1 regulates fragrance biosynthesis in lilies (Lilium spp.)," Molecular breeding, vol. 38, p. 144, 2018.
[39] R. Kurzyna-Młynik, A. A. Oskolski, S. R. Downie, R. Kopacz, A. Wojewódzka, and K. Spalik, "Phylogenetic position of the genus Ferula (Apiaceae) and its placement in tribe Scandiceae as inferred from nrDNA ITS sequence variation," Plant systematics and evolution, vol. 274, p. 47, 2008.
[40] A. Franzke, H. Hurka, D. Janssen, B. Neuffer, N. Friesen, M. Markov, et al., "Molecular signals for Late Tertiary/Early Quaternary range splits of an Eurasian steppe plant: Clausia aprica (Brassicaceae)," Molecular Ecology, vol. 13, pp. 2789-2795, 2004.