Production and gene expression of morphinan alkaloids in hairy root culture of Papaver orientale L. using abiotic elicitors

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• 作者：Seyed Mohammad Hashemi…
• 关键词：Elicitation ; Gene expression ; Hairy root culture ; Morphinan alkaloids ; Papaver orientale L.
• 刊名：Plant Cell, Tissue and Organ Culture
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：125
• 期：1
• 页码：31-41
• 全文大小：1,673 KB
• 参考文献：Allen RS, Miller JAC, Chitty JA, Fist AJ, Gerlach WL, Larkin PJ (2007) Metabolic engineering of morphinan alkaloids by over-expression and RNAi suppression of salutaridinol 7-O-acetyltransferase in opium poppy. Plant Biotechnol J 6:22–30. doi:10.​1111/​j.​1467-7652.​2007.​00293.​x PubMed
  Beaudoin GAW, Facchini PJ (2014) Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240:19–32. doi:10.​1007/​s00425-014-2056-8 CrossRef PubMed
  Broun P, Liu Y, Queen E, Schwarz Y, Abenes ML, Leibman M (2006) Importance of transcription factors in the regulation of plant secondary metabolism and their relevance to the control of terpenoid accumulation. Phytochem Rev 5:27–38. doi:10.​1007/​s11101-006-9000-x CrossRef
  Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395. doi:10.​1007/​s11101-011-9210-8 CrossRef
  Chen J, Shi Y, Liu J (2003) Determination of noradrenaline and dopamine in Chinese herbal extracts from Portulaca oleracea L. by high-performance liquid chromatography. J Chromatogr A 1003:127–132CrossRef PubMed
  Chong TM, Abdullah MA, Lai OM, Nor’Aini FM, Lajis NH (2005) Effective elicitation factors in Morinda elliptica cell suspension culture. Process Biochem 40:3397–3405. doi:10.​1016/​j.​procbio.​2004.​12.​028 CrossRef
  Clark WG, Cline SD, Psenak M, Krueger RJ (1996) Elicitation of dihydrobenzophenanthridine oxidase in Sanguinaria canadensis cell culture. Phytochemistry 43:1141–1144CrossRef PubMed
  Coombs JT, Ritchie JD, Tester MA, Lightfoot D, Jha D (2013) Papaver bracteatum with modified alkaloid content. US Patent Application 13/834,979
  Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. doi:10.​1146/​annurev.​arplant.​48.​1.​355 CrossRef PubMed
  Di Cola A, Costantino P, Spano L (1996) Cell commitment androlB gene expression in the induction of root differentiation. Plant Cell, Tissue Organ Cult 46:203–209CrossRef
  Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274. doi:10.​1016/​S1360-1385(97)86349-2 CrossRef
  Frick S, Kutchan TM (1999) Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis. Plant J 17:329–339CrossRef PubMed
  Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37. doi:10.​1128/​MMBR.​67.​1.​16 CrossRef PubMed PubMedCentral
  Georgiev MI, Kuzeva SL, Pavlov AI, Kovacheva EG, Ilieva MP (2007a) Elicitation of rosmarinic acid by Lavandula vera MM cell suspension culture with abiotic elicitors. World J Microbiol Biotechnol 23:301–304. doi:10.​1007/​s11274-006-9214-5 CrossRef
  Georgiev MI, Pavlov AI, Bley T (2007b) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185. doi:10.​1007/​s00253-007-0856-5 CrossRef PubMed
  Ghorbani M, Ghorbani A, Omidi M, Hashemi SM (2015) Response surface modelling of noradrenaline production in hairy root culture of purslane (Portulaca oleracea L.). Turk J Agric-Food Sci Technol 3:439–443
  Gundlach H, Muller MJ, Kutchan TM, Zenk MH (1992) Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc Natl Acad Sci USA 89:2389–2393CrossRef PubMed PubMedCentral
  Hagel JM, Facchini PJ (2010) Dioxygenases catalyze the O-demethylation steps of morphine biosynthesis in opium poppy. Nat Chem Biol 6:273–275. doi:10.​1038/​nchembio.​317 CrossRef PubMed
  Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G (2014) Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotechnol Appl Biochem 62:24–31. doi:10.​1002/​bab.​1236 CrossRef PubMed
  Hollman A (1996) Drugs for atrial fibrillation. Digoxin comes from Digitalis lanata. BMJ 312:912. doi:10.​1136/​bmj.​312.​7035.​912 CrossRef PubMed PubMedCentral
  Huang F, Kutchan TM (2000) Distribution of morphinan and benzo [c] phenanthridine alkaloid gene transcript accumulation in Papaver somniferum. Phytochemistry 53:555–564CrossRef PubMed
  Kang S, Jung H, Kang Y, Yun D (2004) Effects of methyl jasmonate and salicylic acid on the production of tropane alkaloids and the expression of PMT and H6H in adventitious root cultures of Scopolia parviflora. Plant Sci 166:745–751. doi:10.​1016/​j.​plantsci.​2003.​11.​022 CrossRef
  Kawano N, Kiuchi F, Kawahara N, Yoshimatsu K (2012) Genetic and phenotypic analyses of a Papaver somniferum T-DNA insertional mutant with altered alkaloid composition. Pharmaceuticals 5:133–154. doi:10.​3390/​ph5020133 CrossRef PubMed PubMedCentral
  Khan S, Qureshi MI, Kamaluddin Alam T, Abdin MZ (2007) Protocol for isolation of genomic DNA from dry and fresh roots of medicinal suitable for rapid and restriction digestion. Afr J Biotechnol 6:83–89. doi:10.​3329/​jsr.​v1i3.​2385
  Kim OT, Bang KH, Kim YC, Hyun DY, Kim MY, Cha SW (2009) Upregulation of ginsenoside and gene expression related to triterpene biosynthesis in ginseng hairy root cultures elicited by methyl jasmonate. Plant Cell, Tissue Organ Cult 98:25–33. doi:10.​1007/​s11240-009-9535-9 CrossRef
  Kutchan T (1996) Heterologous expression of alkaloid biosynthetic genes—a review. Gene 179:73–81CrossRef PubMed
  Larkin PJ, Miller JAC, Allen RS, Chitty JA, Gerlach WL, Frick S, Kutchan TM, Fist AJ (2007) Increasing morphinan alkaloid production by over-expressing codeinone reductase in transgenic Papaver somniferum. Plant Biotechnol J 5:26–37. doi:10.​1111/​j.​1467-7652.​2006.​00212.​x CrossRef PubMed
  Le Flem-Bonhomme V, Laurain-Mattar D, Fliniaux MA (2004) Hairy root induction of Papaver somniferum var. album, a difficult-to-transform plant, by A. rhizogenes LBA 9402. Planta 218:890–893. doi:10.​1007/​s00425-003-1196-z CrossRef PubMed
  Liscombe DK, Facchini PJ (2008) Evolutionary and cellular webs in benzylisoquinoline alkaloid biosynthesis. Curr Opin Biotechnol 19:173–180. doi:10.​1016/​j.​copbio.​2008.​02.​012 CrossRef PubMed
  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆cT method. Methods 25:402–408. doi:10.​1006/​meth.​2001.​1262 CrossRef PubMed
  Łuczkiewicz M, Kokotkiewicz A (2005) Co-cultures of shoots and hairy roots of Genista tinctoria L. for synthesis and biotransformation of large amounts of phytoestrogens. Plant Sci 169:862–871. doi:10.​1016/​j.​plantsci.​2005.​06.​005 CrossRef
  Memelink J, Verpoorte R, Kijne JW (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219. doi:10.​1016/​S1360-1385(01)01924-0 CrossRef PubMed
  Mora-Pale M, Sanchez-Rodriguez SP, Linhardt RJ, Dordick JS, Koffas MA (2014) Biochemical strategies for enhancing the in vivo production of natural products with pharmaceutical potential. Curr Opin Biotechnol 25:86–94. doi:10.​1016/​j.​copbio.​2013.​09.​009 CrossRef PubMed
  Namdeo AG (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1:69–79
  Nishimura MT, Stein M, Hou B-H, Vogel JP, Edward H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972. doi:10.​1126/​science.​1086716 CrossRef PubMed
  Nyman U, Bruhn JG (1979) Papaver bracteatum—a summary of current knowledge. Planta Med 35:98–117CrossRef
  Park SU, Facchini PJ (2000) Agrobacterium rhizogenes-mediated transformation of opium poppy, Papaver somniferum L., and california poppy, Eschscholzia californica cham., root cultures. J Exp Bot 51:1005–1016. doi:10.​1093/​jexbot/​51.​347.​1005 CrossRef PubMed
  Patel H, Krishnamurthy R (2013) Elicitors in plant tissue culture. J Pharmacogn Phytochem 2:60–65
  Pichersky E, Lewinsohn E (2011) Convergent evolution in plant specialized metabolism. Annu Rev Plant Biol 62:549–566. doi:10.​1146/​annurev-arplant-042110-103814 CrossRef PubMed
  Queiroz EF, Wolfender J-L, Hostettmann K (2009) Modern approaches in the search for new lead antiparasitic compounds from higher plants. Curr Drug Targets 10:202–211. doi:10.​2174/​1389450097875811​13 CrossRef PubMed
  Ramakrishnan D, Curtis WR (2004) Trickle-bed root culture bioreactor design and scale-up: growth, fluid-dynamics, and oxygen mass transfer. Biotechnol Bioeng 88:248–260. doi:10.​1002/​bit.​20231 CrossRef PubMed
  Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. doi:10.​1038/​nprot.​2008.​73 CrossRef PubMed
  Shafiee A, Lalezari I, Nasseri-nouri P, Asgharian R (1975) Alkaloids of Papaver orientale and Papaver pseudo-orientale. J Pharm Sci 64:9–11
  Sharafi A, Sohi HH, Mousavi A, Azadi P, Khalifani BH, Razavi K (2013a) Metabolic engineering of morphinan alkaloids by over-expression of codeinone reductase in transgenic hairy roots of Papaver bracteatum, the Iranian poppy. Biotechnol Lett 35:445–453. doi:10.​1007/​s10529-012-1080-7 CrossRef PubMed
  Sharafi A, Sohi HH, Mousavi A, Azadi P, Razavi K, Ntui VO (2013b) A reliable and efficient protocol for inducing hairy roots in Papaver bracteatum. Plant Cell, Tissue Organ Cult 113:1–9. doi:10.​1007/​s11240-012-0246-2 CrossRef
  Sharma P, Padh H, Shrivastava N (2013) Hairy root cultures: a suitable biological system for studying secondary metabolic pathways in plants. Eng Life Sci 13:62–75. doi:10.​1002/​elsc.​201200030 CrossRef
  Shoyama Y, Kawachi F, Tanaka H, Nakai R, Shibata T, Nishi K (1998) Genetic and alkaloid analysis of Papaver species and their F1 hybrid by RAPD, HPLC and ELISA. Forensic Sci Int 91:207–217. doi:10.​1016/​S0379-0738(97)00196-5 CrossRef PubMed
  Sivanandhan G, Arun M, Mayavan S, Rajesh M, Jeyaraj M, Dev GK, Manickavasagam M, Selvaraj N, Ganapathi A (2012) Optimization of elicitation conditions with methyl jasmonate and salicylic acid to improve the productivity of withanolides in the adventitious root culture of Withania somnifera (L.) dunal. Appl Biochem Biotechnol 168:681–696. doi:10.​1007/​s12010-012-9809-2 CrossRef PubMed
  Sivanandhan G, Kapil G, Murugaraj D (2013) Increased production of withanolide A, withanone, and withaferin A in hairy root cultures of Withania somnifera (L.) Dunal elicited with methyl jasmonate and salicylic acid. Plant Cell, Tissue Organ Cult 114:121–129. doi:10.​1007/​s11240-013-0297-z CrossRef
  Souret FF, Kim Y, Wyslouzil BE, Wobbe KK, Weathers PJ (2003) Scale-up of Artemisia annua L. hairy root cultures produces complex patterns of terpenoid gene expression. Biotechnol Bioeng 83:653–667. doi:10.​1002/​bit.​10711 CrossRef PubMed
  Sudha CG, Sherina TV, Anu Anand VP, Reji JV, Padmesh P, Soniya EV (2013) Agrobacterium rhizogenes mediated transformation of the medicinal plant Decalepis arayalpathra and production of 2-hydroxy-4-methoxy benzaldehyde. Plant Cell, Tissue Organ Cult 112:217–226. doi:10.​1007/​s11240-012-0226-6 CrossRef
  Szabady ZSB, Cirnpan MSG, Nyiredy S (2011) High-throughput analytical strategy with combined planar and column liquid chromatography for improvement of the poppy (Papaver somniferum L.) with a high alkaloid content. Chromatographia 56:49–54
  Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374. doi:10.​1007/​s10529-010-0417-3 CrossRef PubMed
  Verma P, Khan SA, Mathur AK, Ghosh S, Shanker K, Kalra A (2014) Improved sanguinarine production via biotic and abiotic elicitations and precursor feeding in cell suspensions of latex-less variety of Papaver somniferum with their gene expression studies and upscaling in bioreactor. Protoplasma 3:1359–1371. doi:10.​1007/​s00709-014-0638-8 CrossRef
  Wahby I, Caba JM, Ligero F (2013) Agrobacterium infection of hemp (Cannabis sativa L.): establishment of hairy root cultures. J Plant Interact 8:312–320. doi:10.​1080/​17429145.​2012.​746399 CrossRef
  WHO (1993) World health organization (WHO) Geneva, Switzerland and Worldwide Fund for Nature Gland, Switzerland
  Wijekoon CP, Facchini PJ (2012) Systematic knockdown of morphine pathway enzymes in opium poppy using virus-induced gene silencing. Plant J 69:1052–1063. doi:10.​1111/​j.​1365-313X.​2011.​04855.​x CrossRef PubMed
  Zang Y, Zheng W, He Y, Hong SB, Zhu Z (2015) Global analysis of transcriptional response of Chinese cabbage to methyl jasmonate reveals JA signaling on enhancement of secondary metabolism pathways. Sci Hortic 189:159–167. doi:10.​1016/​j.​scienta.​2015.​04.​008 CrossRef
  Zare N, Farjaminezhad R, Asghari-Zakaria R, Farjaminezhad M (2014) Enhanced thebaine production in Papaver bracteatum cell suspension culture by combination of elicitation and precursor feeding. Nat Prod Res 28:711–717. doi:10.​1080/​14786419.​2013.​878936 CrossRef PubMed
  Ziegler J, Voigtländer S, Schmidt J, Kramell R, Miersch O, Ammer C, Gesell A, Kutchan TM (2006) Comparative transcript and alkaloid profiling in Papaver species identifies a short chain dehydrogenase/reductase involved in morphine biosynthesis. Plant J 48:177–192. doi:10.​1111/​j.​1365-313X.​2006.​02860.​x CrossRef PubMed
  
• 作者单位：Seyed Mohammad Hashemi (1)
  Mohammad Reza Naghavi (1)
  
  1. Department of Agronomy and Plant Breeding, College of Agriculture and Natural Resources, University of Tehran, Tehran, Iran
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Plant Sciences
  Plant Physiology
  
• 出版者：Springer Netherlands
• ISSN：1573-5044

文摘

Nowadays, hairy root culture elicitation is an excellent platform with many advantages which make it an attractive system for using in plant biochemistry and molecular biology. Here, an efficient system for A. rhizogenes transformation in oriental poppy, Papaver orientale, was developed. Meanwhile, the expression level of various genes (COR, SalAT, SalR, T6ODM, CODM and Salsyn) in the morphinan pathway for response to methyl jasmonate (MJ) and salicylic acid (SA) at different time points (6, 12, 24 and 48 h) was examined. Afterwards, in vitro production of thebaine, morphine and codeine was investigated. The wild-type A. rhizogenes strain ATCC15834 was able to produce transformed roots with the highest frequency on the hypocotyl explant. Quantitative reverse-transcription PCR analysis showed that the expression of SalR, Salsyn, SalAT, T6ODM and CODM were significantly up-regulated with MJ treatment at 48 h. Moreover, the expression levels of Salsyn, T6ODM and CODM was up-regulated considerably in SA at 48 h treatment, while, the expression of SalR was down-regulated at 24 h. Furthermore, high-performance liquid chromatography analysis showed that MJ elicitation enhanced thebaine and morphine at 48 h by 2.63-fold (3.08 mg g−1) and 6.18-fold (5.38 mg g−1), respectively, and also codeine was increased at 24 h by 3.67-fold (2.57 mg g−1). In addition, the accumulation of morphine and thebaine was increased by 4.22-fold (2.87 mg g−1) and 2-fold (1.66 mg g−1) in comparison with control treatment after SA treatment for 48 h. Our findings suggest that oriental poppy hairy roots can be used as a good source for producing commercial alkaloids.