Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-14T11:16:02.549Z Has data issue: false hasContentIssue false
  • English
  • Français

Medicinal plant transcriptomes: the new gateways for accelerated understanding of plant secondary metabolism

Part of: Evolving Trends in Plant Based Drug Discovery

Published online by Cambridge University Press:  16 June 2016

Sandhya Tripathi ,
Jyoti Singh Jadaun ,
Muktesh Chandra  and
Neelam S. Sangwan
Sandhya Tripathi
Affiliation:
Metabolic and Structural Biology Department, CSIR-Central Institute for Medicinal and Aromatic Plants (CSIR-CIMAP), Lucknow-226015, UP, India
Jyoti Singh Jadaun
Affiliation:
Metabolic and Structural Biology Department, CSIR-Central Institute for Medicinal and Aromatic Plants (CSIR-CIMAP), Lucknow-226015, UP, India
Muktesh Chandra
Affiliation:
Metabolic and Structural Biology Department, CSIR-Central Institute for Medicinal and Aromatic Plants (CSIR-CIMAP), Lucknow-226015, UP, India
Neelam S. Sangwan*
Affiliation:
Metabolic and Structural Biology Department, CSIR-Central Institute for Medicinal and Aromatic Plants (CSIR-CIMAP), Lucknow-226015, UP, India
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Medicinal plants are the vital source of numerous structurally diverse pharmacologically active metabolites collectively called as secondary metabolites finding extensive applications in traditional systems of medicine and in pharmaceutical industries. Several distinctive and complex pathways operate in an interactive manner via metabolic networks that are responsible for the accumulation of such highly specialized metabolites. Secondary metabolites are believed to play a wide spectrum of physiological and functional roles in plants, many of which being investigated and supported by the experimental studies. Biosynthetic pathway related studies on various aspects in these medicinal plants have been found very tedious owing to several issues in plants such as considerably lower metabolite concentrations in native tissues, existence at different locations, and highly complex multi-step pathways, etc. Pathway elucidation and gene/enzyme discovery for studying metabolic pathway evolution and subsequent engineering could be better achieved by mining various pathway databases and reconstruction of metabolic networks available at different omics databases. Though medicinal plants have a limited range of genomic sequences available, however recently, next generation sequencing is being widely used to generate a comprehensive transcriptomic resource for these plants. It is anticipated that databases and resources generated from these studies are likely to play a key role towards the study and exploitation of metabolites from medicinal plants in near future. In this review, we have discussed next generation sequencing approaches, which were used for the generation of transcriptomic resources for several medicinally important plants. The relevance of transcriptomic approaches in curation of the pathways linked with the synthesis of major secondary metabolites along with their precursors of pharmaceutical importance in medicinal plants is also comprehensively analysed.

Keywords

ashwagandhaNGSessential oilsplant secondary metabolismterpenoidstranscriptome
Type
Research Article
Information
Plant Genetic Resources , Volume 14 , Special Issue 4: Evolving trends in plant based drug discovery , December 2016 , pp. 256 - 269
Copyright
Copyright © NIAB 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, MD, Soares, MB, Kerlavage, AR, Fields, C and Venter, JC (1993) Rapid cDNA sequencing (expressed sequence tags) from a directionally cloned human infant brain cDNA library. Nature Genetics 4: 373–380.CrossRefGoogle ScholarPubMed
Alagna, F, D'Agostino, N, Torchia, L, Servili, M, Rao, R, Pietrella, M and Perrotta, G (2009) Comparative 454 pyrosequencing of transcripts from two olive genotypes during fruit development. BMC Genomics 10: 399.Google Scholar
Annadurai, RS, Jayakumar, V, Mugasimangalam, RC, Katta, M, Anand, S, Gopinathan, S, Sarma, SP, Fernandes, SJ, Mullapudi, N, Murugesan, S and Rao, SN (2012) Next generation sequencing and de novo transcriptome analysis of Costus pictus D. Don, a non-model plant with potent anti-diabetic properties. BMC Genomics 13: 663.CrossRefGoogle Scholar
Barrero, RA, Chapman, B, Yang, Y, Moolhuijzen, P, Keeble-Gagnère, G, Zhang, N and Qiu, D (2011) De novo assembly of Euphorbia fischeriana root transcriptome identifies prostratin pathway related genes. BMC Genomics 12: 600.Google Scholar
Bentley, DR, Balasubramanian, S, Swerdlow, HP, Smith, GP, Milton, J, Brown, CG, Hall, KP, Evers, DJ, Barnes, CL, Bignell, HR and Anastasi, C (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 4567: 53–59.CrossRefGoogle Scholar
Borevitz, JO, Xia, Y, Blount, J, Dixon, RA, Lamb, C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. The Plant Cell 12: 2383–2394.Google Scholar
Bose, SK, Yadav, RK, Mishra, S, Sangwan, RS, Singh, AK, Mishra, B, Srivastava, AK and Sangwan, NS (2013) Effects of gibberellic acid and calliterpenone on plant growth attributes, trichomes, essential oil biosynthesis and pathway gene expression in differential manner in Menthaarvensis L. Plant Physiology and Biochemistry 66: 150–158.Google Scholar
Bose Mazumdar, A and Chattopadhyay, S (2016) Sequencing, de novo assembly, functional annotation and analysis of Phyllanthus amarus leaf transcriptome using the Illumina platform. Frontiers in Plant Science 6: 1199.CrossRefGoogle ScholarPubMed
Brautigam, A, Mullick, T, Schliesky, S and Weber, AP (2011) Critical assessment of assembly strategies for non-model species mRNA-Seq data and application of next-generation sequencing to the comparison of C3 and C4 species. Journal of Experimental Botany 62: 3093–3102.CrossRefGoogle Scholar
Celenza, JL, Quiel, JA, Smolen, GA, Merrikh, H, Silvestro, AR, Normanly, J and Bender, J (2005) The Arabidopsis ATR1 Myb transcription factor controls indolicglucosinolate homeostasis. Plant physiology 137: 253–262.Google Scholar
Chaurasiya, ND, Sangwan, RS, Misra, LN, Tuli, R and Sangwan, NS (2009) Metabolic clustering of a core collection of Indian ginseng Withania somnifera Dunal through DNA, isoenzyme, polypeptide and withanolide profile diversity. Fitoterapia 80: 496–505.CrossRefGoogle ScholarPubMed
Chen, S, Luo, H, Li, Y, Sun, Y, Wu, Q, Niu, Y, Song, J, Lv, A, Zhu, Y and Sun, C (2011) 454 EST analysis detects genes putatively involved in ginsenoside biosynthesis in Panax ginseng . Plant Cell Reports 30: 1593–1601.Google Scholar
Chen, J, Hou, K, Qin, P, Liu, H, Yi, B, Yang, W and Wu, W (2014) RNA-Seq for gene identification and transcript profiling of three Stevia rebaudiana genotypes. BMC Genomics 15: 571.CrossRefGoogle ScholarPubMed
Chevreux, B, Pfisterer, T, Drescher, B, Driesel, AJ, Müller, WE, Wetter, T and Suhai, S (2004) Using the mira EST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research 14: 1147–1159.Google Scholar
Chowhan, N, Singh, HP, Batish, DR, Kaur, S, Ahuja, N, Kohli, RK (2013) β- Pinene inhibited germination and early growth involves membrane peroxidation. Protoplasma 250: 691–700 CrossRefGoogle ScholarPubMed
Collins, LJ, Biggs, PJ, Voelckel, C and Joly, S (2008) An approach to transcriptome analysis of non-model organisms using short-read sequences. Genome Informatics 21: 3–14.Google Scholar
Conesa, A and Götz, S (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. International journal of plant genomics 2008: 619832.Google Scholar
Conesa, A, Götz, S, García-Gómez, JM, Terol, J, Talón, M and Robles, M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676.CrossRefGoogle ScholarPubMed
Cooke, B and Ernst, E (2000) Aromatherapy: a systematic review. British Journal of General Practice 50: 493–496.Google Scholar
Dasgupta, MG, George, BS, Bhatia, A and Sidhu, OP (2014) Characterization of Withania somnifera leaf transcriptome and expression analysis of pathogenesis–related genes during salicylic acid signaling. PloS one 9(4): 94803Google Scholar
De Bernonville, TD, Foureau, E, Parage, C, Lanoue, A, Clastre, M, Londono, MA, Oudin, A, Houillé, B, Papon, N, Besseau, S and Glévarec, G (2015) Characterization of a second secologanin synthase isoform producing both secologanin and secoxyloganin allows enhanced de novo assembly of a Catharanthus roseus transcriptome. BMC Genomics 16: 619.CrossRefGoogle Scholar
Deluc, L, Barrieu, F, Marchive, C, Lauvergeat, V, Decendit, A, Richard, T, Carde, JP, Mérillon, JM and Hamdi, S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant physiology 140(2): 499–511.Google Scholar
Deng, N, Chang, E, Li, M, Ji, J, Yao, X, Bartish, IV, Liu, J, Ma, J, Chen, L, Jiang, Z and Shi, S (2016) Transcriptome characterization of Gnetum parvifolium reveals candidate genes involved in important secondary metabolic pathways of flavonoids and stilbenoids. Frontiers in Plant Science 4: 174.Google Scholar
Denoeud, F, Aury, JM, Da Silva, C, Noel, B, Rogier, O, Delledonne, M and Artiguenave, F (2008) Annotating genomes with massive-scale RNA sequencing. Genome Biology 9: R175.CrossRefGoogle ScholarPubMed
Egan, AN, Schlueter, J and Spooner, DM (2012) Applications of next-generation sequencing in plant biology. American Journal of Botany 99: 175–185.Google Scholar
Espley, RV, Hellens, RP, Putterill, J, Stevenson, DE, Kutty-Amma, S and Allan, AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. The Plant Journal 49: 414–427.Google Scholar
Fan, R, Li, Y, Li, C and Zhang, Y (2015) Differential microRNA analysis of glandular trichomes and young leaves in xanthium strumarium L. reveals their putative roles in regulating terpenoid biosynthesis. PLoS ONE 10: e0139002.Google Scholar
Fakari, FR, Tabatabaeichehr, M, Kamali, H, Fakari, FR and Naseri, M (2015) Effect of inhalation of aroma of geranium essence on anxiety and physiological parameters during first stage of labor in nulliparous women: a randomized clinical trial. Journal of Caring Sciences 4: 135.Google Scholar
Galla, G, Volpato, M, Sharbel, TF and Barcaccia, G (2013) Computational identification of conserved microRNAs and their putative targets in the Hypericumperforatum L. flowertranscriptome. Plant Reproduction 26: 209–229.CrossRefGoogle Scholar
Garber, M, Grabherr, MG, Guttman, M and Trapnell, C (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nature methods 8(6): 469–477 Google Scholar
Garg, A, Agrawal, L, Misra, RC, Sharma, S and Ghosh, S (2015) Andrographis paniculata transcriptome provides molecular insights into tissue-specific accumulation of medicinal diterpenes. BMC Genomics 16: 659.CrossRefGoogle ScholarPubMed
Garg, R, Patel, RK, Tyagi, AK and Jain, M (2011) De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA research 18(1): 53–63.Google Scholar
Góngora-Castillo, E, Fedewa, G, Yeo, Y, Chappell, J, DellaPenna, D and Buell, CR (2012) Genomic approaches for interrogating the biochemistry of medicinal plant species. Methods in Enzymology 517: 139.Google Scholar
Götz, S, García-Gómez, JM, Terol, J, Williams, TD, Nagaraj, SH, Nueda, MJ and Conesa, A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Research 36: 3420–3435.Google Scholar
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I and Regev, A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644–652.Google Scholar
Grotewold, E, Drummond, BJ, Bowen, B and Peterson, T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.Google Scholar
Guo, X, Li, Y, Li, C, Luo, H, Wang, L, Qian, J, Luo, X, Xiang, L, Song, J, Sun, C, Xu, H, Yao, H and Chen, S (2013) Analysis of the Dendrobium officinale transcriptome reveals putative alkaloid biosynthetic genes and genetic markers. Gene 527: 131–138.Google Scholar
Guo, Q, Ma, X, Wei, S, Qiu, D, Wilson, IW, Wu, P, Tang, Q, Liu, L, Dong, S and Zu, W (2014) De novo transcriptome sequencing and digital gene expression analysis predict biosynthetic pathway of rhynchophylline and isorhynchophylline from Uncariarhynchophylla, a non-model plant with potent anti-alzheimer's properties. BMC Genomics 15: 676.CrossRefGoogle Scholar
Gupta, P, Goel, R, Agarwal, AV, Asif, MH, Sangwan, NS, Sangwan, RS and Trivedi, PK. (2015) Comparative transcriptome analysis of different chemotypes elucidates withanolide biosynthesis pathway from medicinal plant Withania somnifera. Sci Rep 21(5): 18611Google Scholar
Gupta, P, Goel, R, Pathak, S, Srivastava, A, Singh, SP, Sangwan, RS and Trivedi, PK (2013) De novo assembly functional annotation and comparative analysis of Withania somnifera leaf and root transcriptomes to identify putative genes involved in the withanolides biosynthesis. PLoS ONE 8: e62714.CrossRefGoogle ScholarPubMed
Hao, D, Ma, P, Mu, J, Chen, S, Xiao, P, Peng, Y and Sun, C (2012) De novo characterization of the root transcriptome of a traditional Chinese medicinal plant Polygonum cuspidatum . Science China Life Sciences 55: 452–466.Google Scholar
He, M, Wang, Y, Hua, W, Zhang, Y and Wang, Z (2012) De novo sequencing of Hypericum perforatum transcriptome to identify potential genes involved in the biosynthesis of active metabolites. PLoS ONE 7: e42081.Google Scholar
Huang, X and Madan, A (1999) CAP3: A DNA sequence assembly program. Genome research 9: 868–877.Google Scholar
Hwang, HS, Lee, H and Choi, YE (2015) Transcriptomic analysis of Siberian ginseng (Eleutherococcus senticosus) to discover genes involved in saponin biosynthesis. BMC Genomics 16: 1.Google Scholar
Jadaun, JS, Sangwan, NS, Narnoliya, LK, Tripathi, S and Sangwan, RS (2016) Withania coagulans tryptophan decarboxylase gene cloning, heterologous expression and catalytic characteristics of the recombinant enzyme. Protoplasma 1–12.Google Scholar
Jacobs, DI, Gaspari, M, van der Greef, J, van der Heijden, R and Verpoorte, R (2005) Proteome analysis of the medicinal plant Catharanthus roseus. Planta 221(5): 690–704.Google Scholar
Jain, M, Srivastava, PL, Verma, M, Ghangal, R and Garg, R (2016) De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. Scientific Reports 6: 22456.Google Scholar
Korkina, L, Kostyuk, V, De Luca, C and Pastore, S (2011) Plant phenylpropanoids as emerging anti-inflammatory agents. Mini Reviews in Medicinal Chemistry 11: 823–835.CrossRefGoogle ScholarPubMed
Krishnan, NM, Pattnaik, S, Jain, P, Gaur, P, Choudhary, R, Vaidyanathan, S, Deepak, S, Hariharan, AK, Krishna, PGB, Nair, J, Varghese, L, Valivarthi, NK, Dhas, K, Ramaswamy, K and Panda, B (2012) A draft of the genome and four transcriptomes of a medicinal and pesticidal angiosperm Azadirachta indica . BMC Genomics 13: 464–477.CrossRefGoogle ScholarPubMed
Kumar, R, Sangwan, RS, Mishra, S, Sabir, F and Sangwan, NS (2012) In silico motif diversity analysis of the glycon preferentiality of plant secondary metabolic glycosyltransferases. Plant Omics Journal 5: 200–210.Google Scholar
Kushwaha, AK, Sangwan, NS, Tripathi, S and Sangwan, RS (2013) Molecular cloning and catalytic characterization of a recombinant tropine biosynthetic tropinone reductase from Withania coagulans leaf. Gene 516: 238–247.Google Scholar
Lee, GW, Lee, B, Chung, MS, Jeong, YS, Chung, BY (2015) Rice terpene synthase 20 (OsTPS20) plays an important role in producing terpene volatiles in response to abiotic stresses. Protoplasma 252(4): 997–1007.Google Scholar
Li, H and Durbin, R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25: 1754–1760.Google Scholar
Li, C, Zhu, Y, Guo, X, Sun, C, Luo, H, Song, J, Li, Y, Wang, L, Qian, J and Chen, S. (2013) Transcriptome analysis reveals ginsenosides biosynthetic genes, microRNAs and simple sequence repeats in Panax ginseng C. A. Meyer. BMC Genomics 14: 245–256.Google Scholar
Liu, T, Zhu, S, Tang, Q, Chen, P, Yu, Y and Tang, S (2013) De novo assembly and characterization of transcriptome using Illumina paired-end sequencing and identification of CesA gene in ramie (Boehmerianivea L. Gaud). BMC Genomics 14: 125.Google Scholar
Luo, H, Sun, C, Sun, Y, Wu, Q, Li, Y, Song, J, Niu, Y, Cheng, X, Xu, H, Li, C, Liu, J, Steinmetz, A and Chen, S (2011) Analysis of the transcriptome of Panax notoginseng root uncovers putative triterpene saponin-biosynthetic genes and genetic markers. BMC Genomics 12:1.Google Scholar
Luo, R, Liu, B, Xie, Y, Li, Z, Huang, W, Yuan, J and Wang, J (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1: 18.CrossRefGoogle ScholarPubMed
Maher, CA, Kumar-Sinha, C, Cao, X, Kalyana-Sundaram, S, Han, B, Jing, X and Chinnaiyan, AM (2009) Transcriptome sequencing to detect gene fusions in cancer. Nature 458: 97–101.Google Scholar
Margulies, M, Egholm, M, Altman, WE, Attiya, S, Bader, JS, Bemben, LA and Volkmer, GA (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376–380.Google Scholar
Martin, J, Bruno, VM, Fang, Z, Meng, X, Blow, M, Zhang, T, Sherlock, G, Snyder, M and Wang, Z (2010) Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads. BMC genomics 11(1): 663CrossRefGoogle ScholarPubMed
Marshall, JC, Vincent, JL, Fink, MP, Cook, DJ, Rubenfeld, G, Foster, D, Fisher, CJ Jr, Faist, E and Reinhart, K (2003) Measures, markers, and mediators: toward a staging system for clinical sepsis. A report of the Fifth Toronto Sepsis Roundtable, Toronto, Ontario, Canada. Critical care medicine 31( 5): 1560–1567.Google Scholar
McKerrow, JH (2015) Recognition of the role of Natural Products as drugs to treat neglected tropical diseases by the 2015 Nobel prize in physiology or medicine. Natural product reports 32(12): 1610–1.CrossRefGoogle ScholarPubMed
McKernan, KJ, Peckham, HE, Costa, GL, McLaughlin, SF, Fu, Y, Tsung, EF and Blanchard, AP (2009) Sequence and structural variation in a human genome uncovered by short-read, massively parallel ligation sequencing using two-base encoding. Genome Research 19: 1527–1541.Google Scholar
Mishra, S, Bansal, S, Mishra, B, Sangwan, RS, Asha, , Jadaun, JS and Sangwan, NS (2016) RNAi and homologous over-expression based functional approaches reveal triterpenoid synthase gene-cycloartenol synthase is involved in downstream withanolide biosynthesis in Withania somnifera . PLoS ONE 11: e0149691. doi: 10.1371/journal.pone.0149691.Google Scholar
Mishra, S, Bansal, S, Sangwan, RS and Sangwan, NS (2015) Genotype independent and efficient Agrobacterium-mediated genetic transformation of the medicinal plant Withania somnifera Dunal. Journal of Plant Biochemistry and Biotechnology: 1–8.Google Scholar
Mitsuda, N, Seki, M, Shinozaki, K and Ohme-Takagi, M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17: 2993–3006.Google Scholar
Moerkercke, AV, Fabris, M, Pollier, J, Baart, GJ, Rombauts, S, Hasnain, G, Rischer, H, Memelink, J, Oksman-Caldentey, KM and Goossens, A (2013) CathaCyc, a metabolic pathway database built from Catharanthus roseus RNA-Seq Data. Plant Cell Physiol. 54: 673–85.Google Scholar
Mondal, S, Bandyopadhyay, SK, Ghosh, M, Mukhopadhyay, S, Roy, S and Mandal, C (2012) Natural products: promising resources for cancer drug discovery. Anti-Cancer Agents in Medicinal Chemistry (Formerly Current Medicinal Chemistry-Anti-Cancer Agents) 12(1): 49–75.Google Scholar
Narnoliya, LK, Rajakani, R, Sangwan, NS, Gupta, V and Sangwan, RS (2014) Comparative transcripts profiling of fruit mesocarp and endocarp relevant to secondary metabolism by suppression subtractive hybridization in Azadirachta indica(neem). Molecular Biology Reports 41: 3147–3162.Google Scholar
Nick, P (2015) Perfumes of survival. Protoplasma. 252: 933–934.Google Scholar
Odimegwu, JI, Odukoya, O, Yadav, RK, Chanotiya, CS, Ogbonnia, S and Sangwan, NS (2013) A New Source of Elemol Rich Essential Oil and Existence of Multicellular Oil Glands in Leaves of the Dioscorea Species. The Scientific World Journal 2013: 943598.Google Scholar
Oksman-Caldentey, KM, Inze, D and Orešič, M (2004) Connecting genes to metabolites by a systems biology approach. Proceedings of the National Academy of Sciences of the United States of America 101: 9949–9950.Google Scholar
Pan, Q, Saiman, MZ, Mustafa, NR, Verpoorte, R and Tang, K (2016) A simple and rapid HPLC-DAD method for simultaneously monitoring the accumulation of alkaloids and precursors in different parts and different developmental stages of Catharanthus roseus plants. Journal of Chromatography 55:.Google Scholar
Parchman, TL, Geist, KS, Grahnen, JA, Benkman, CW and Buerkle, CA (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC genomics 11(1): 1 CrossRefGoogle Scholar
Park, S, Ruhlman, TA, Sabir, JS, Mutwakil, MH, Baeshen, MN, Sabir, MJ, Baeshen, NA and Jansen, RK (2014) Complete sequences of organelle genomes from the medicinal plant Rhazyastricta (Apocynaceae) and contrasting patterns of mitochondrial genome evolution across asterids. BMC Genomics 15: 405.Google Scholar
Prakash, P, Rajakani, R and Gupta, V (2016) Transcriptome-wide identification of Rauvolfia serpentina microRNAs and prediction of their potential targets. Computational Biology and Chemistry 61: 62.Google Scholar
Rajakani, R, Narnoliya, L, Sangwan, NS, Sangwan, RS and Gupta, V (2014) Subtractive transcriptomes of fruit and leaf reveal differential representation of transcripts in Azadirachta indica . Tree Genetics & Genomes 10: 1331–1351.Google Scholar
Rastogi, S, Meena, S, Bhattacharya, A, Ghosh, S, Shukla, RK, Sangwan, NS, Lal, RK, Gupta, MM, Lavania, UC, Gupta, V, Nagegowda, DA and Shasany, AK (2014) De novo sequencing and comparative analysis of holy and sweet basil transcriptomes. BMC Genomics 15: 588–606.Google Scholar
Robertson, G, Schein, J, Chiu, R, Corbett, R, Field, M, Jackman, SD and Birol, I (2010) De novo assembly and analysis of RNA-seq data. Nature methods 7: 909–912.Google Scholar
Sabir, F, Mishra, S, Sangwan, RS, Jadaun, JS and Sangwan, NS (2013) Qualitative and quantitative variations in withanolides and expression of some pathway genes during different stages of morphogenesis in Withania somnifera Dunal. Protoplasma 250(2): 539–549.CrossRefGoogle ScholarPubMed
Sangwan, NS and Sangwan, RS (2014) Secondary metabolites of traditional medical plants: a case study of Ashwagandha (Withania somnifera). Applied Plant Cell Biology 22: 325–367.CrossRefGoogle Scholar
Sangwan, NS, Yadav, U and Sangwan, RS (2003) Genetic diversity among elite varieties of the aromatic grasses, Cymbopogon martinii. Euphytica 130(1): 117–130.Google Scholar
Sangwan, RS, Chaurasiya, ND, Lal, P, Misra, L, Tuli, R and Sangwan, NS (2008) Withanolide A is inherently de novo biosynthesized in roots of the medicinal plant Ashwagandha (Withania somnifera). Physiologia Plantarum 133: 278–287.Google Scholar
Sangwan, NS, Kumar, R, Srivastava, S, Kumar, A, Gupta, A and Sangwan, RS (2010) Recent developments on secondary metabolite biosynthesis in Artemisia annuaL. Journal of Plant Biology 37: 1–24.Google Scholar
Sangwan, RS, Tripathi, S, Singh, J, Narnoliya, L and Sangwan, NS (2013) De novo sequencing and assembly of Centella asiatica leaf transcriptome for mapping of structural, functional and regulatory genes with special reference to secondary metabolism. Gene 525: 58–76.Google Scholar
Sangwan, NS, Mishra, LN, Tripathi, S, Kushwaha, AK and Sangwan, RS (2014) Omics of secondary metabolic pathways in Withania somnifera Dunal (ashwagandha). OMICS Applications In Crop Science 385–408.Google Scholar
Sangwan, NS, Tiwari, P, Mishra, SK, Yadav, RK, Tripathi, S, Kushwaha, AK and Sangwan, RS (2015) Plant Metabolomics: An Overview of Technology Platforms for Applications in Metabolism. InPlantOmics: The Omics of Plant Science: 257–298.Google Scholar
Senthil, K, Jayakodi, M, Thirugnanasambantham, P, Lee, SC, Duraisamy, P, Purushotham, PM and Yang, TJ (2015) Transcriptome analysis reveals in vitro cultured Withania somnifera leaf and root tissues as a promising source for targeted withanolide biosynthesis. BMC genomics 16: 14.Google Scholar
Sharma, S, Sangwan, NS and Sangwan, RS (2003) Developmental process of essential oil glandular trichome collapsing in menthol mint. Current science 84(4): 544–550.Google Scholar
Sharma, PC, Jain, A and Chaudhary, S (2012) Transcriptome Analysis in Seabuckthorn (Hippophae rhamnoides L.), a medicinally important plant. In International Conference on Environmental and Biological Sciences Conference.Google Scholar
Singh, J, Farzana, S, Sangwan, RS, Narnoliya, LK and Sangwan, NS (2014) Enhanced secondary metabolite production and pathway gene expression by leaf explants-induced direct root morphotypes are regulated by combination of growth regulators and culture conditions in Centellaasiatica (L.) urban. Plant Growth Regulation 75: 55–66.Google Scholar
Singh Sangwan, N, Abad Farooqi, AH and Sangwan, RS (1994) Effect of drought stress on growth and essential oil metabolism in lemongrasses. New Phytologist 128: 173–179.Google Scholar
Skirycz, A, Jozefczuk, S, Stobiecki, M, Muth, D, Zanor, MI, Witt, I and Mueller-Roeber, B (2007) Transcription factor AtDOF4; 2 affects phenylpropanoid metabolism in Arabidopsis thaliana. New Phytologist 175: 425–438 Google Scholar
Soetaert, SS, Van Neste, CM, Vandewoestyne, ML, Head, SR, Goossens, A, Van Nieuwerburgh, FC and Deforce, DL (2013) Differential transcriptome analysis of glandular and filamentous trichomes in Artemisia annua . BMC Plant Biology 13: 220.Google Scholar
Spyropoulou, EA, Haring, MA and Schuurink, RC (2014) RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters. BMC genomics 15(1): 1Google Scholar
Srivastava, S and Sangwan, RS (2012) Analysis of Artemisia annua transcriptome for BAHD alcohol acyltransferase genes: identification and diversity of expression in leaf, stem and root. Journal of Plant Biochemistry and Biotechnology 21: 108–118.Google Scholar
Srivastava, S, Sangwan, RS, Tripathi, S, Mishra, B, Narnoliya, LK, Misra, LN and Sangwan, NS (2015) Light and auxin responsive cytochrome P450s from Withania somnifera Dunal: cloning, expression and molecular modelling of two pairs of homologue genes with differential regulation. Protoplasma 256(6):1421–1437.CrossRefGoogle Scholar
Stracke, R, Werber, M and Weisshaar, B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Current opinion in plant biology 4: 447–456.Google Scholar
Sui, C, Chen, M, Xu, J, Wei, J, Jin, Y, Xu, Y, Sun, J, Gao, K, Yang, C, Zhang, Z, Chen, S and Luo, H (2015) Comparison of root transcriptomes and expressions of genes involved in main medicinal secondary metabolites from Bupleurum chinense and Bupleurum scorzonerifolium, the two Chinese official Radix bupleuri source species. Plant Physiology 153: 230–242.Google Scholar
Sui, C, Zhang, J, Wei, J, Chen, S, Li, Y, Xu, J, Jin, Y, Xie, C, Gao, Z, Chen, H, Yang, C, Zhang, Z and Xu, Y (2011) Transcriptome analysis of Bupleurum chinense focusing on genes involved in the biosynthesis of saikosaponins. BMC Genomics 12(1):539.Google Scholar
Sun, C, Li, Y, Wu, Q, Luo, H and Sun, Y (2010) De novo sequencing and analysis of the American ginseng root transcriptome using a GS FLX titanium platform to discover putative genes involved in ginsenoside biosynthesis. BMC Genomics 11: 262.Google Scholar
Sun, Y, Luo, H, Li, Y, Sun, C, Song, J, Niu, Y, Zhu, Y, Dong, L, Lv, A, Tramontano, E and Chen, S (2011) Pyrosequencing of the Camptotheca acuminate transcriptome reveals putative genes involved in camptothecin biosynthesis and transport. BMC Genomics 12: 533–543.CrossRefGoogle Scholar
Sun, Y, Luo, H, Li, Y, Sun, C, Song, J, Niu, Y, Zhu, Y, Dong, L, Lv, A, Tramontano, E and Chen, S (2012) Pyrosequencing of the Camptotheca acuminatetranscriptome reveals putative genes involved in camptothecin biosynthesis and transport. BMC Genomics 12: 533–543.Google Scholar
Sunohara, Y, Baba, Y, Matsuyama, S, Fujimura, K, Matsumoto, H (2015) Screening and identification of phytotoxic volatile compounds in medicinal plants, and characterizations of a selected compound, eucarvone. Protoplasma 252(4): 1047–59.Google Scholar
Thiel, T, Michalek, W, Varshney, RK and Graner, A (2003) Exploiting EST 941 databases for the development and characterization of gene derived SSR markers in barley (Hordeumvulgare L.). Theoretical and Applied Genetics 106: 411–422.Google Scholar
Tiwari, P, Sangwan, RS, Asha, , Mishra, BN, Sabir, F and Sangwan, NS (2014) Molecular cloning and Biochemical characterization of a recombinant 3-O-glucosyltransferase from Gymnemasylvestre R.Br. catalyzing biosynthesis of sterylglucosides. Biomed Research International doi: 10.1155/2014/934351.CrossRefGoogle Scholar
Upadhyay, S, Phukan, UJ, Mishra, S and Shukla, RK (2014) De novo leaf and root transcriptome analysis identified novel genes involved in Steroidal sapogenin biosynthesis in Asparagus racemosus . BMC Genomics 15: 746.Google Scholar
Van Der Fits, L and Memelink, J (2001) The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. The Plant Journal 25: 43–53.Google Scholar
Verdonk, JC, Haring, MA, van Tunen, AJ and Schuurink, RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. The Plant Cell Online 17: 1612–1624.Google Scholar
VomEndt, D, Kijne, JW and Memelink, J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators? Phytochemistry 61: 107–114.Google Scholar
Wagner, GJ, Wang, E and Shepherd, RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93: 3–11.Google Scholar
Waites, R, Selvadurai, HR, Oliver, IR and Hudson, A (1998) The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93: 779–789.Google Scholar
Wang, ET, Sandberg, R, Luo, S, Khrebtukova, I, Zhang, L, Mayr, C and Burge, CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470–476.Google Scholar
Wang, W, Wang, Y, Zhang, Q, Qi, Y and Guo, D (2009) Global characterization of Artemisia annua glandular trichometranscriptome using 454 pyrosequencing. BMC Genomics 10: 465.Google Scholar
Wang, LH, Lin, YP and Lin, YC (2016) Screening nicotinamide in cosmetic and pharmaceutical products and nicotinic acid skin penetration from essential-oil formulations using attenuated total reflectance-infrared spectroscopy. Biomedical Spectroscopy and Imaging 5: 89–97.Google Scholar
Wang, Z, Fang, B, Chen, J, Zhang, X, Luo, Z, Huang, L and Li, Y (2010) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweet potato (Ipomoea batatas). BMC genomics 11: 726.Google Scholar
Wenping, H, Yuan, Z, Jie, S, Lijun, Z and Zhezhi, W (2011) De novo transcriptome sequencing in Salvia miltiorrhiza to identify genes involved in the biosynthesis of active ingredients. Genomics 98: 272–279.Google Scholar
Wu, B, Wang, M, Ma, Y, Yuan, L and Lu, S (2012) High-throughput sequencing and characterization of the small RNA transcriptome reveal features of novel and conserved microRNAs in Panax ginseng. PLoS ONE 7: e44385.Google ScholarPubMed
Wu, HQ, Wang, L, Guo, W, Gao, XX, Bai, L and Zhang, WM (2013) High-quality total RNA extraction from medicinal plant Aquilaria sinensis . Zhong Yao Cai 36: 1055–1059.Google Scholar
Wu, Q, Sun, C, Luo, H, Li, Y, Niu, Y, Sun, Y, Lu, A and Chen, S (2011) Transcriptome analysis of Taxus cuspidate needles based on 454 pyrosequencing. Planta Medica 77: 394–400.Google Scholar
Xiao, M, Zhang, Y, Chen, X, Lee, EJ, Barber, CJ, Chakrabarty, R, Desgagné-Penix, I, Haslam, TM, Kim, YB, Liu, E and MacNevin, G (2013) Transcriptome analysis based on next-generation sequencing of non-model plants producing specialized metabolites of biotechnological interest. Journal of Biotechnology 166: 122–134.Google Scholar
Xia, Z, Xu, H, Zhai, J, Li, D, Luo, H, He, C and Huang, X (2011) RNA-Seq analysis and de novo transcriptome assembly of Heveabrasiliensis. Plant Molecular Biology 77: 299–308 Google Scholar
Xie, T, Wang, S, Huang, L, Wang, X, Kang, LP and Guo, LP (2014) Transcriptome-based bioinformatics analysis of Arnebia euchroma ERF transcription factor family. ZhongguoZhong Yao ZaZhi 39: 4732–4739.Google Scholar
Xu, YH, Wang, JW, Wang, S, Wang, JY and Chen, XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene ( + )-δ-cadinene synthase-A. Plant Physiology 135(1): 507–515.Google Scholar
Yadav, RK, Sangwan, RS, Srivastava, AK, Maurya, S and Sangwan, NS (2013) Comparative profiling and dynamics of artemisnin related metabolites using efficient protocol and expression of biosynthetic pathway genes during developmental span of two elite varieties of Artemisia annua L. Journal of Plant Biochemistry and Biotechnology 24(2):167–175.Google Scholar
Yadav, RK, Sangwan, RS, Sabir, F, Srivastava, AK and Sangwan, NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiology and Biochemistry 74C: 70–83.Google Scholar
Yamazaki, M, Mochida, K, Asano, T, Nakabayashi, R, Chiba, M, Udomson, N, Yamazaki, Y, Goodenowe, DB, Sankawa, U, Yoshida, T and Toyoda, A (2013) Coupling deep transcriptome analysis with untargeted metabolic profiling in Ophiorrhiza pumila to further the understanding of the biosynthesis of the anti-cancer alkaloid camptothecin and anthraquinones. Plant and cell physiology 54(5): 686–96.Google Scholar
Yang, L, Ding, G, Lin, H, Cheng, H and Kong, Y (2013) Transcriptome analysis of medicinal plant Salvia miltiorrhiza and identification of genes related to tanshinone biosynthesis. PLoS ONE 8: e80464.Google Scholar
Zeng, S, Xiao, G, Guo, J, Fei, Z, Xu, Y, Roe, BA and Wang, Y (2010) Development of a EST dataset and characterization of EST-SSRs in a traditional Chinese medicinal plant, Epimedium sagittatum (Sieb. Et Zucc.) Maxim. BMC genomics 11(1): 1Google Scholar
Zhao, S, Tuan, PA, Li, X, Kim, YB, Kim, H, Park, CG, Yang, J, Li, CH and Park, SU (2013) Identification of phenylpropanoid biosynthetic genes and phenylpropanoid accumulation by transcriptome analysis of Lyciumchinense. BMC Genomics 14: 802.Google Scholar
Zheng, X, Pan, C, Diao, Y, You, Y, Yang, C and Hu, Z (2013) Development of microsatellite markers by transcriptome sequencing in two species of Amorphophallus (Araceae). BMC Genomics 14: 490.Google Scholar
Zheng, X, Xu, H, Ma, X, Zhan, R, Chen, W (2014) Triterpenoidsaponin biosynthetic pathway profiling and candidate gene mining of the Ilex asprella root using RNA-Seq. Int J Mol Sci 15(4): 5970–87.Google Scholar
Zerbino, DR and Birney, E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18: 821–829.Google Scholar