Transcriptome sequencing of rhizome tissue of Sinopodophyllum hexandrum at two temperatures

BMC Genomics

Sanjay Kumar²  Ravi Shankar³  Mohit Kumar Swarnkar²  Ashwani Jha¹  Heikham Russiachand Singh³  Anita Kumari¹ 

[1] Academy of Scientific & Innovative Research, New Delhi, India;Biotechnology Division, CSIR-Institute of Himalayan Bioresource Technology, PO Box No. 6, Palampur 176 061, Himachal Pradesh, India;Studio of Computational Biology & Bioinformatics, CSIR-Institute of Himalayan Bioresource Technology, PO Box No. 6, Palampur 176 061, Himachal Pradesh, India

关键词: Stress;    RNA-seq;    Podophyllotoxin;    Next generation sequencing;    Growth;    Gene expression;    Development;    Deep sequencing;    Below ground;   

Others  :  1130617
DOI  :  10.1186/1471-2164-15-871

 received in 2013-12-26, accepted in 2014-09-17,  发布年份 2014

【 摘 要 】

Background

Sinopodophyllum hexandrum is an endangered medicinal herb, which is commonly present in elevations ranging between 2,400–4,500 m and is sensitive to temperature. Medicinal property of the species is attributed to the presence of podophyllotoxin in the rhizome tissue. The present work analyzed transcriptome of rhizome tissue of S. hexandrum exposed to 15°C and 25°C to understand the temperature mediated molecular responses including those associated with podophyllotoxin biosynthesis.

Results

Deep sequencing of transcriptome with an average coverage of 88.34X yielded 60,089 assembled transcript sequences representing 20,387 unique genes having homology to known genes. Fragments per kilobase of exon per million fragments mapped (FPKM) based expression analysis revealed genes related to growth and development were over-expressed at 15°C, whereas genes involved in stress response were over-expressed at 25°C. There was a decreasing trend of podophyllotoxin accumulation at 25°C; data was well supported by the expression of corresponding genes of the pathway. FPKM data was validated by quantitative real-time polymerase chain reaction data using a total of thirty four genes and a positive correlation between the two platforms of gene expression was obtained. Also, detailed analyses yielded cytochrome P450s, methyltransferases and glycosyltransferases which could be the potential candidate hitherto unidentified genes of podophyllotoxin biosynthesis pathway.

Conclusions

The present work revealed temperature responsive transcriptome of S. hexandrum on Illumina platform. Data suggested expression of genes for growth and development and podophyllotoxin biosynthesis at 15°C, and prevalence of those associated with stress response at 25°C.

【 授权许可】

   
2014 Kumari et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Shaw JMH: New combinations for the varieties of Sinopodophyllum hexandrum. Hanburyana 2009, 4:33-39.
• [2]Stähelin HF, von Wartburg A: The chemical and biological route from podophyllotoxin glucoside to etoposide: ninth Cain memorial Award lecture. Cancer Res 1991, 51:5-15.
• [3]Nadeem M, Palni LMS, Purohit AN, Pandey H, Nandi SK: Propagation and conservation of Podophyllum hexandrum Royle: an important medicinal herb. Biol Conserv 2000, 92:121-129.
• [4]Giri A, Lakshmi Narasu M: Production of podophyllotoxin from Podophyllum hexandrum: a potential natural product for clinically useful anticancer drugs. Cytotechnology 2000, 34:17-26.
• [5]You Y: Podophyllotoxin derivatives: current synthetic approaches for new anticancer agents. Curr Pharm Des 2005, 11:1695-1717.
• [6]Kim E, Donohue K: Local adaptation and plasticity of Erysimum capitatum to altitude: its implications for responses to climate change. J Ecol 2013, 101:796-805.
• [7]Kushwaha R, Pandey S, Chanda S, Bhattacharya A, Ahuja PS: Temperature dependent growth and emergence of functional leaves: an adaptive mechanism in the seedlings of the western Himalayan plant Podophyllum hexandrum. J Plant Res 2008, 121:299-309.
• [8]Singh A, Purohit AN: Light and temperature effects on physiological reactions on alpine and temperate populations of Podophyllum hexandrum Royle. J Herbs Spices Med Plants 1997, 5:57-66.
• [9]Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP: Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 2004, 40:173-187.
• [10]Derory J, Léger P, Garcia V, Schaeffer J, Hauser MT, Salin F, Luschnig C, Plomion C, Glössl J, Kremer A: Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol 2006, 170:723-738.
• [11]Paul A, Kumar S: Responses to winter dormancy, temperature, and plant hormones share gene networks. Funct Integr Genomics 2011, 11:659-664.
• [12]Gahlan P, Singh HR, Shankar R, Sharma N, Kumari A, Chawla V, Ahuja PS, Kumar S: De novo sequencing and characterization of Picrorhiza kurrooa transcriptome at two temperatures showed major transcriptome adjustments. BMC Genomics 2012, 13:126. BioMed Central Full Text
• [13]Venkataraman K: India’s Biodiversity Act 2002 and its role in conservation. Trop Ecol 2009, 50:23-30.
• [14]Bhattacharyya D, Sinha R, Ghanta S, Chakraborty A, Hazra S, Chattopadhyay S: Proteins differentially expressed in elicited cell suspension culture of Podophyllum hexandrum with enhanced podophyllotoxin content. Proteome Sci 2012, 10:34. BioMed Central Full Text
• [15]Sultan P, Shawl AS, Abdellah AA, Ramteke PW: Isolation, Characterization and Comparative Study on Podophyllotoxin and Related Glycosides of Podophyllum heaxandrum. Curr Res J Biol Sci 2010, 2:345-351.
• [16]Marques JV, Kim KW, Lee C, Costa MA, May GD, Crow JA, Davin LB, Lewis NG: Next generation sequencing in predicting gene function in podophyllotoxin biosynthesis. J Biol Chem 2013, 288:466-479.
• [17]Compound extraction of Podophyllum peltatum [http://uic.edu/pharmacy/MedPlTranscriptome/d_podo_p_3.html webcite]
• [18]Muoki RC, Paul A, Kumari A, Singh K, Kumar S: An improved protocol for the isolation of RNA from roots of tea (Camellia sinensis (L.) O. Kuntze). Mol Biotechnol 2012, 52:82-88.
• [19]GenScript real-time PCR primer design [https://www.genscript.com/ssl-bin/app/primer webcite]
• [20]Pfaffl WP, Horgan GW, Dempfle L: Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
• [21]Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J: De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2009, 20:265-272.
• [22]Li W, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22:1658-1659.
• [23]UniProt Consortium: Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2011, 40(Database issue):D71-D75.
• [24]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29.
• [25]Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M: KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 1999, 27:29-34.
• [26]Webb EC: International Union of Biochemistry and Molecular Biology. Nomenclature Committee. Enzyme nomenclature: Recommendations of the Nomenclature Committee of the International Union of Biochemistry and Molecular Biology on the nomenclature and classification of enzymes. San Diego: Academic Press; 1992:862.
• [27]Schmid R, Blaxter ML: annot8r: GO, EC and KEGG annotation of EST datasets. BMC Bioinformatics 2008, 9:180. BioMed Central Full Text
• [28]Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B: PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 2010, 40(Database issue):D822-D827.
• [29]Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW: The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 2004, 32:5539-5545.
• [30]Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E: The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 2012, 40(Database issue):D1202-D1210.
• [31]Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH: CDD: a Conserved domain database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:225-229.
• [32]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-seq. Bioinformatics 2009, 25:1105-1111.
• [33]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515.
• [34]MISA Program [http://pgrc.ipk-gatersleben.de/misa webcite]
• [35]Zhang P, Dreher K, Karthikeyan A, Chi A, Pujar A, Caspi R, Karp P, Kirkup V, Latendresse M, Lee C, Mueller LA, Muller R, Rhee SY: Creation of a genome-wide metabolic pathway database for Populus trichocarpa using a new approach for reconstruction and curation of metabolic pathways for plants. Plant Physiol 2010, 153:1479-1491.
• [36]Salick J, Fangb Z, Byg A: Eastern Himalayan alpine plant ecology, Tibetan ethnobotany, and climate change. Global Environ Chang 2009, 19:147-155.
• [37]Zobayed SM, Afreen F, Kozai T: Temperature stress can alter the photosynthetic efficiency and secondary metabolite concentrations in St. John’s wort. Plant Physiol Biochem 2005, 43:977-984.
• [38]Alam MA, Gulati P, Aswini KG, Gyan PM, Pradeep KN: Assessment of genetic diversity among Podophyllum hexandrum genotypes of northwestern Himalayan region for podophyllotoxin production. Indian J Biotechnol 2009, 8:391-399.
• [39]Chandra S: Effect of altitude on energy exchange characteristics of some alpine medicinal crops from central Himalayas. J Agron Crop Sci 2004, 190:13-20.
• [40]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [41]Vinogradov AE: DNA helix: the importance of being GC-rich. Nucleic Acids Res 2003, 31:1838-1844.
• [42]Nestor CE, Monckton DG: Correlation of inter-locus polyglutamine toxicity with CAG•CTG triplet repeat expandability and flanking genomic DNA GC content. PLoS One 2011, 6:e28260.
• [43]Holland JB, Helland SJ, Sharopova N, Rhyne DC: Polymorphism of PCR-based markers targeting exons, introns, promoter regions, and SSRs in maize and introns and repeat sequences in oat. Genome 2001, 44:1065-1076.
• [44]Musashi M, Ota S, Shiroshita N: The role of protein kinase C isoforms in cell proliferation and apoptosis. Int J Hematol 2000, 72:12-19.
• [45]Annadurai RS, Jayakumar V, Mugasimangalam RC, Katta MA, Anand S, Gopinathan S, Sarma SP, Fernandes SJ, Mullapudi N, Murugesan S, Rao SN: Next generation sequencing and de novo transcriptome analysis of Costus pictus D. Don, a non-model plant with potent anti-diabetic properties. BMC Genomics 2012, 13:663. BioMed Central Full Text
• [46]Smith IK, Polle A, Rennenberg H: Glutathione. In Stress Responses in Plants: Adaptation and Acclimation Mechanisms. Edited by Alscher RG, Cumming JR. New York: Wiley Liss Inc; 1992:201-215.
• [47]Vu JCV, Allen LH Jr, Gesch RW: Up-regulation of photosynthesis and sucrose metabolism enzymes in young expanding leaves of sugarcane under elevated growth CO2. Plant Sci 2006, 171:123-131.
• [48]An D, Yang J, Zhang P: Transcriptome profiling of low temperature treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genomics 2012, 13:64. BioMed Central Full Text
• [49]Hotton SK, Callis J: Regulation of cullin RING ligases. Annu Rev Plant Biol 2008, 59:467-489.
• [50]TAIR [https://www.arabidopsis.org/servlets/TairObject?name=AT3G12670&type=locus webcite]
• [51]Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E: Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 2005, 139:509-518.
• [52]Ha CM, Jun JH, Nam HG, Fletcher JC: BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 2004, 45:1361-1370.
• [53]Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK: Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 1994, 6:1211-1225.
• [54]Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G: Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 2000, 288:1613-1616.
• [55]Kim WC, Reca IB, Kim Y, Park S, Thomashow MF, Keegstra K, Han KH: Transcription factors that directly regulate the expression of CSLA9 encoding mannan synthase in Arabidopsis thaliana. Plant Mol Biol 2014, 84:577-587.
• [56]Apuya NR, Yadegari R, Fischer RL, Harada JJ, Zimmerman JL, Goldberg RB: The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60alpha gene. Plant Physiol 2001, 126:717-730.
• [57]Davletova S, Schlauch K, Coutu J, Mittler R: The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 2005, 139:847-856.
• [58]Polidoros AN, Mylona PV, Pasentsis K, Scandalios JG, Tsaftaris AS: The maize alternative oxidase 1a (Aox1a) gene is regulated by signals related to oxidative stress. Redox Rep 2005, 10:71-78.
• [59]Diédhiou CJ, Popova OV, Dietz KJ, Golldack D: The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 2008, 8:49. BioMed Central Full Text
• [60]Wang W, Vinocur B, Shoseyov O, Altman A: Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004, 9:244-252.
• [61]Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K: AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 2012, 1819:86-96.
• [62]Yi Y, Guerinot ML: Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 1996, 10:835-844.
• [63]Sun S, Yu JP, Chen F, Zhao TJ, Fang XH, Li YQ, Sui SF: TINY, a dehydration-responsive element (DRE)-binding protein-like transcription factor connecting the DRE- and ethylene-responsive element-mediated signaling pathways in Arabidopsis. J Biol Chem 2008, 283:6261-6271.
• [64]Wang J, Chen L, Huang S, Liu J, Ren X, Tian X, Qiao J, Zhang W: RNA-seq based identification and mutant validation of gene targets related to ethanol resistance in cyanobacterial Synechocystis sp. PCC 6803. Biotechnol Biofuels 2012, 5:89. BioMed Central Full Text
• [65]Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X: Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 2011, 62:5607-5621.
• [66]Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC: The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 2003, 20:735-747.
• [67]Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L: MYB transcription factors in Arabidopsis. Trends Plant Sci 2010, 15:573-581.
• [68]Bienz M: The PHD finger, a nuclear protein-interaction domain. Trends Biochem Sci 2006, 31:35-40.
• [69]Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K: Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 2004, 16:2481-2498.
• [70]Englbrecht CC, Schoof H, Böhm S: Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 2004, 5:39. BioMed Central Full Text
• [71]Jackson DE, Dewick PM: Biosynthesis of Podophyllum lignans-II. Interconversion of aryltetralin lignans in Podophyllum hexandrum. Phytochemistry 1984, 23:1037-1042.
• [72]Hoffmann L, Maury S, Martz F, Geoffroy P, Legrand M: Purification, cloning and properties of an acyltransferase controlling shikimate and quinate ester intermediates in phenylpropanoid metabolism. J Biol Chem 2003, 278:95-103.
• [73]Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D: CYP98A3 from Arabidopsis thaliana is a 3′-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 2001, 276:36566-36574.
• [74]Fraser CM, Chapple C: The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 2011, 9:e0152.
• [75]Davin LB, Wang HB, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG: Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 1997, 275:362-366.
• [76]Katayama T, Davin LB, Lewis NG: An extraordinary accumulation of (-)-pinoresinol in cell-free extracts of Forsythia intermedia: evidence for enantiospecific reduction of (+)-pinoresinol. Phytochemistry 1992, 31:3875-3881.
• [77]Katayama T, Davin LB, Chu A, Lewis NG: Novel benzylic ether reductions in lignan biogenesis in Forsythia intermedia. Phytochemistry 1993, 33:581-591.
• [78]Umezawa T, Davin LB, Lewis NG: Formation of lignans, (-)-secoisolariciresinol and (-)-matairesinol with Forsythia intermedia cell-free extracts. J Biol Chem 1991, 266:10210-10217.
• [79]Sakakibara N, Suzuki S, Umezawa T, Shimada M: Biosynthesis of yatein in Anthriscus sylvestris. Org Biomol Chem 2003, 1:2474-2485.
• [80]Broomhead AJ, Rahman MA, Dewick PM, Jackson DE, Lucas JA: Matairesinol as precursor of Podophyllum lignans. Phytochemistry 1991, 30:1489-1492.
• [81]Kuhlmann S, Kranz K, Lücking B: Aspects of cytotoxic lignan biosynthesis in suspension cultures of Linum nodiflorum. Phytochem Rev 2002, 1:37-43.
• [82]Kamil WM, Dewick PM: Biosynthesis of the lignans α- and β-peltatin. Phytochemistry 1986, 25:2089-2092.
• [83]van Uden W, Bouma AS, Bracht Waker JF, Middel O, Wichers HJ, Waard PD, Woerdenbag HJ, Kellogg RM, Pras N: The production of podophyllotoxin and its 5-methoxy derivative through bioconversion of cyclodextrin complexed deoxy-podophyllotoxin by plant cell cultures. Plant Cell Tissue Organ Cult 1995, 42:73-79.
• [84]van Uden W, Bos JA, Boeke GM, Woerdenbag HJ, Pras N: The large-scale isolation of deoxypodophyllotoxin from rhizomes of Anthriscus sylvestris followed by its bioconversion into 5-methoxypodophyllotoxin β-d-glucoside by cell cultures of Linun flavum. J Natural Prod 1997, 60:401-403.
• [85]Yousefzadi M, Sharifi M, Behmanesh M, Moyano E, Bonfill M, Cusido RM, Palazon J: Podophyllotoxin: current approaches to its biotechnological production and future challenges. Eng Life Sci 2010, 10:281-292.
• [86]Singh K, Rani A, Paul A, Dutt S, Joshi R, Gulati A, Ahuja PS, Kumar S: Differential display mediated cloning of anthocyanidin reductase gene from tea (Camellia sinensis) and its relationship with the concentration of epicatechins. Tree Physiol 2009, 29:837-846.
• [87]Kawoosa T, Singh H, Kumar A, Sharma SK, Devi K, Dutt S, Vats SK, Sharma M, Ahuja PS, Kumar S: Light and temperature regulated terpene biosynthesis: hepatoprotective monoterpene picroside accumulation in Picrorhiza kurrooa. Funct Integr Genomics 2010, 10:393-404.
• [88]Kumar H, Singh K, Kumar S: 2C-methyl-d-erythritol-2,4-cyclodiphosphate synthase from Stevia rebaudiana Bertoni is a functional gene. Mol Biol Rep 2012, 12:10971-10978.
• [89]Singh RS, Gara RK, Bhardwaj PK, Kaachra A, Malik S, Kumar R, Sharma M, Ahuja PS, Kumar S: Expression of 3-hydroxy-3-methylglutaryl-CoA reductase, p-hydroxybenzoate-m-geranyltransferase and genes of phenylpropanoid pathway exhibits positive correlation with shikonins content in arnebia [Arnebia euchroma (Royle) Johnston]. BMC Mol Biol 2010, 11:88. BioMed Central Full Text
• [90]Schuler MA: Plant cytochrome P450 monooxygenases. Crit Rev Plant Sci 1996, 15:235-284.
• [91]Federolf K, Alfermann AW, Fuss E: Aryltetralin-lignan formation in two different cell suspension cultures of Linum album: Deoxypodophyllotoxin 6-hydroxylase, a key-enzyme in the formation of 6-methoxypodophyllotoxin. Phytochemistry 2007, 68:1397-1406.
• [92]Lam KC, Ibrahim RK, Behdad B, Dayanandan S: Structure, function, and evolution of plant O-methyltransferases. Genome 2007, 50:1001-1013.
• [93]Lewis NG, Yamamoto E: Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 1990, 41:455-496.
• [94]Boerjan W, Ralph J, Baucher M: Lignin biosynthesis. Annu Rev Plant Biol 2003, 54:519-546.
• [95]Zhong R, Morrison WH III, Himmelsbach DS, Poole FL II, Ye ZH: Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol 2000, 124:563-578.
• [96]Ross J, Li Y, Lim E, Bowles DJ: Higher plant glycosyltransferases. Genome Biol 2001, 2:REVIEWS3004.
• [97]Vogt T, Jones P: Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci 2000, 5:380-386.
• [98]Wang J, Hou B: Glycosyltransferases: key players involved in the modification of plant secondary metabolites. Front Biol China 2009, 4:39-46.
• [99]Berim A, Ebel R, Schneider B, Petersen M: UDP-glucose:(6-methoxy) podophyllotoxin 7-O-glucosyltransferase from suspension cultures of Linum nodiflorum. Phytochemistry 2008, 69:374-381.
• [100]Jha A, Mehra M, Shankar R: The regulatory epicenter of miRNAs. J Biosci 2011, 36:621-638.
• [101]Jha A, Shankar R: miReader: Discovering novel miRNAs in species without sequenced genome. PLoS One 2013, 8:e66857.