Abstract
Plants display an amazing ability to synthesize a vast array of secondary metabolites that are an inexhaustible source of phytochemicals, bioactive molecules some of which impact the human health. Phytochemicals present in medicinal herbs and spices have long been used as natural remedies against illness. Plant tissue culture represents an alternative to whole plants as a source of phytochemicals. This approach spares agricultural land that can be used for producing food and other raw materials, thus favoring standardized phytochemical production regardless of climatic adversities and political events. Over the past 20 years, different strategies have been developed to increase the synthesis and the extraction of phytochemicals from tissue culture often obtaining remarkable results. Moreover, the availability of genomics and metabolomics tools, along with improved recombinant methods related to the ability to overexpress, silence or disrupt one or more genes of the pathway of interest promise to open new exciting possibilities of metabolic engineering. This review provides a general framework of the cellular and molecular tools developed so far to enhance the yield of phytochemicals. Additionally, some emerging topics such as the culture of cambial meristemoid cells, the selection of plant cell following the expression of genes encoding human target proteins, and the bioextraction of phytochemicals from plant material have been addressed. Altogether, the herein described techniques and results are expected to improve metabolic engineering tools aiming at improving the production of phytochemicals of pharmaceutical and nutraceutical interest.
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References
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 6:30910. https://doi.org/10.1038/srep30910
Alavizadeh SH, Hosseinzadeh H (2014) Bioactivity assessment and toxicity of crocin: a comprehensive review. Food Chem Toxicol 64:65–80. https://doi.org/10.1016/j.fct.2013.11.016
Ambid C, Fallot J (1981) Role of the gaseous environment on volatile compounds production by fruit cell suspension cultures in vitro. In: Scherir (ed) Proceedings of the international conference on flavour, 3rd Weurman symposium De Gruyter, Berlin, New York, pp 529–538
Arencibia AD, Aleydis Gómez A, Mora P, Orellana F, Alarcón JE (2018) Photomixotrophic cultures of blueberries (Vaccinium corymbosum) accumulate or release phenylpropanoids via inductive treatments. Acta Physiol Plant 40:36. https://doi.org/10.1007/s11738-018-2615-x
Aronson JK (2017) Defining nutraceuticals: neither nutritious nor pharmaceuticals. Br J Clin Pharmacol 83:8–19. https://doi.org/10.1111/bcp.12935
Baiano A (2014) Recovery of biomolecules from food wastes—a review. Molecules 19(9):14821–14842. https://doi.org/10.3390/molecules190914821
Baikenova GG, Abdulina GA, Gazaliev AM, Fazylov SD, Kudaibergenova SZ (2004) Synthesis and antimicrobial activity of anabasine, piperidine, and morpholine dithiocarbamates. Pharm Chem J 38(1):19–20. https://doi.org/10.1023/b:phac.0000027638.24327.bd
Balathandayutham K, Cheruth AJ, Changxing Z, Melvin JM, Jothi S, Muthukumar D (2008) The effect of AM fungi and phosphorous level on the biomass yield and ajmalicine production in Catharanthus roseus. Eur J Biosci 2:26–33
Balažová A, Urdová J, Bilka F, Holková I, Horváth B, Forman V, Mučaji P (2018) Evaluation of manganese chloride’s effect on biosynthetic properties of in vitro cultures of Eschscholzia californica Cham. Molecules 23:971. https://doi.org/10.3390/molecules23040971
Bauer N, Vuković R, Likić S, Jelaska S (2015) Potential of different Coleus blumei tissues for rosmarinic acid production. Food Technol Biotechnol 53:3–10. https://doi.org/10.17113/ftb.53.01.15.3661
Beaudoin GA, Facchini PJ (2014) Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240:19–32. https://doi.org/10.1007/s00425-014-2056-8
Beiderbeck R, Knoop B (1984) Ein adsorbens als Speicher fur phytohormone in einer pflantzlichen suspensionkulture. Z Naturforsch. 39c:45–49. https://doi.org/10.1515/znc-1984-1-208
Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2016) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84. https://doi.org/10.1016/j.copbio.2014.11.007
Berlin J, Sieg S, Strack D, Bokern M, Harms H (1986) Production of betalains by suspension cultures of Chenopodium rubrum L. Plant Cell Tissue Org Cult 5:163–174. https://doi.org/10.1007/bf00040126
Bobak M, Nádaska M, Samaj J, Blehova A, Erdelsky K, Ovecka M, Kristín J (1995) The influence of elicitation on the subcellular localization and content of sanguinarine in callus cells of Papaver somniferum L. Biol Plant 37(4):501–506. https://doi.org/10.1007/bf02908827
Boke H, Ozhuner E, Turktas M, Parmaksiz I, Ozcan S, Turgay Unver T (2015) Regulation of the alkaloid biosynthesis by miRNA in opium poppy. Plant Biotechnol J 13:409–420
Bortesi L, Fischer R (2014) The CRISPR–Cas9 system for plant genome editing and beyond. Biotechnol Adv 33:41–52. https://doi.org/10.1016/j.biotechadv.2014.12.006
Bovy A, De Vos R, Kemper M, Schijlen E, Almenar Pertejo M, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S, Santos-Buelga C, Van Tunen A (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526. https://doi.org/10.1105/tpc.004218
Brown DP, Rogers DT, Gunjan SK, Gerhardt GA, Littleton JM (2016) Target-directed discovery and production of pharmaceuticals in transgenic mutant plant cells. J Biotechnol 238:9–14. https://doi.org/10.1016/j.jbiotec.2016.09.007
Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Jie Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308. https://doi.org/10.1038/nbt.1506
Caleja C, Barreiro MF, Ferreira I (2017) Phenolic compounds as nutraceuticals or functional food ingredients. Curr Pharm Des 23:2787–2806. https://doi.org/10.2174/1381612822666161227153906
Caretto S, Quarta A, Durante M, Nisi R, De Paolis A, Blando F, Mita G (2011) Methyl jasmonate and miconazole differently affect arteminisin production and gene expression in Artemisia annua suspension cultures. Plant Biol 13:51–58. https://doi.org/10.1111/j.1438-8677.2009.00306.x
Chandini SK, Rao LJ, Gowthaman MK, Haware DJ, Subramanian R (2011) Enzymatic treatment to improve the quality of black tea extracts. Food Chem 127:1039–1045. https://doi.org/10.1016/j.foodchem.2011.01.078
Chandler SF, Dodds JH (1983) The effect of phosphate, nitrogen and sucrose on the production of phenolics and solasodine in callus cultures of Solanum laciniatum. Plant Cell Rep 2(4):205–208. https://doi.org/10.1007/bf00270105
Chattopadhyay S, Srivastava AK, Bisaria VS (2004) Production of phytochemicals in plant cell bioreactors. Plant Biotechnol Mol Mark. https://doi.org/10.1007/1-4020-3213-7_7
Chen ZY, Jiao R, Ma KY (2008) Cholesterol-lowering nutraceuticals and functional foods. J Agric Food Chem 56:8761–8773. https://doi.org/10.1021/jf801566r
Chen K, Shan Q, Gao C (2014a) An efficient TALEN mutagenesis system in rice. Methods 69:2–8. https://doi.org/10.1016/j.ymeth.2014.02.013
Chen G, Wang H, Zhang X, Yang ST (2014b) Nutraceuticals and functional foods in the management of hyperlipidemia, critical reviews. Food Sci Nutr 54:1180–1201. https://doi.org/10.1080/10408398.2011.629354
Chintapakorn Y, Hamill JD (2011) Antisense-mediated down-regulation of putrescine N-methyltransferase activity in transgenic Nicotiana tabacum L. can lead to elevated levels of anatabine at the expense of nicotine. Plant Mol Biol 53:87–105. https://doi.org/10.1023/b:plan.0000009268.45851.95
Chouhan S, Sharma K, Zha J, Guleria S, Koffas MAG (2017) Recent advances in the recombinant biosynthesis of polyphenols. Front Microbiol 8:22–59. https://doi.org/10.3389/fmicb.2017.02259 (eCollection 2017)
Chukwumah YC, Walker LT, Verghese M, Ogutu S (2009) Effect of frequency and duration of ultrasonication on the extraction efficiency of selected isoflavones andtrans-resveratrol from peanuts (Arachis hypogaea). Ultrason Sonochem 16:293–299. https://doi.org/10.1016/j.ultsonch.2008.07.007
Corchete MP, Sanchez JM, Cacho M, Moran M, Fernandez-Tarrago J (1990) Cardenolide content in suspension cell cultures derived from root and leaf callus of Digitalis thapsi L. J Plant Physiol 137:196–200. https://doi.org/10.1016/s0176-1617(11)80081-7
Costa C, Tsatsakis A, Mamoulakis C, Teodoro M, Briguglio G, Caruso E, Tsoukalas D, Margina D, Dardiotis E, Kouretas D, Fenga C (2017) Current evidence on the effect of dietary polyphenols intake on chronic diseases. Food Chem Toxicol 110:286–299. https://doi.org/10.1016/j.fct.2017.10.023
Courtois D, Guern J (1980) Temperature response of Catharanthus roseus cells cultivated in liquid medium. Plant Sci Lett 17:473–482. https://doi.org/10.1016/0304-4211(80)90135-2
DeBoer KD, Dalton HL, Edward FJ, Hamill JD (2011) RNAi-mediated down-regulation of ornithine decarboxylase (ODC) leads to reduced nicotine and increased anatabine levels in transgenic Nicotiana tabacum L. Phytochemistry 72:344–355. https://doi.org/10.1016/j.phytochem.2010.12.012
Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guiot R, Pietrella M et al (2014) The coffee genome provides insight into the convergent evolution of caggeine biosynthesis. Science 345:1181–1184
Desagagné-Penix I, Facchini PJ (2012) Systematic silencing of benzylisoquinoline alkaloid biosynthetic genes reveals the major route to papaverine in opium poppy. Plant J 72:331–334. https://doi.org/10.1111/j.1365-313x.2012.05084.x
Diretto G, Al-Babili S, Tavazza R, Papacchioli V, Beyer P, Giuliano G (2007) Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS One 2:e350. https://doi.org/10.1371/journal.pone.0000350
Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, Beyer P, Giuliano G (2010) Transcriptional-metabolic networks in β-carotene-enriched potato tubers: the long and winding road to the golden phenotype. Plant Physiol 154:899–912. https://doi.org/10.1104/pp.110.159368
Dixon RA, Steele CL (1999) Flavonoids and isoflavonoids—a gold mine for metabolic engineering. Trends Plant Sci 4(10):394–400. https://doi.org/10.1016/S1360-1385(99)01471-5
Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR–Cas9. Science 346:1258096. https://doi.org/10.1126/science.1258096
Dougall DK, Johnson JM, Whitten GH (1980) A clonal analysis of anthocyanin accumulation by cell cultures of wild carrot. Planta 149:292–297. https://doi.org/10.1007/bf00384569
Efferth T (2018) Biotechnology applications of plant callus cultures. Engineering. https://doi.org/10.1016/j.eng.2018.11.006
Eibl R, Eibl D (2008) Design of bioreactors suitable for plant cell and tissue cultures. Phytoc Rev 7:593–598. https://doi.org/10.1007/s11101-007-9083-z
Fett-Neto AG, Melanson SJ, Nicholson SA, Jason J, Pennington JJ, Di Cosmo F (1994) Improved taxol yield by aromatic carboxylic acid and amino acid feeding to cell cultures of Taxus cuspidate. Biotechnol Bioeng 44:967–971. https://doi.org/10.1002/bit.260440813
Forkmann G, Stefan Martens S (2001) Metabolic engineering and applications of flavonoids. Curr Opin Biotechnol 12:155–160. https://doi.org/10.1016/s0958-1669(00)00192-0
Fu R, Martin C, Zhang Y (2018) Next-generation plant metabolic engineering inspired by ancient Chinese irrigation system. Mol Pant 11:47–57. https://doi.org/10.1016/j.molp.2017.09.002
Furze JM, Rhodes MJ, Parr AJ, Robins RJ, Withehead IM, Threlfall DR (1991) Abiotic factors elicit sesquiterpenoid phytoalexin production but not alkaloid production in transformed root cultures of Datura stramonium. Plant Cell Rep 10(3):111–114. https://doi.org/10.1007/bf00232039
Gajowik A, Dobrzyńska MM (2014) Lycopene-antioxidant with radioprotective and anticancer properties. A review. Rocz Panstw Zakl Hig 65:263–271
Gantet P, Memelink J (2002) Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. Trends Pharmacol Sci 23:563–569. https://doi.org/10.1016/S0165-6147(02)02098
Geipel K, Song X, Socher ML, Kümmritz S, Püschel J, Bley T, Ludwig-Müller J, Steingroewer J (2014) Induction of a photomixotrophic plant cell culture of Helianthus annuus and optimization of culture conditions for improved α-tocopherol production. Appl Microbiol Biotechnol 98:2029–2040. https://doi.org/10.1007/s00253-013-5431-7
Georgiev MI, Eibl R, Zhong JJ (2013) Hosting the plant cells in vitro: recent trends in bioreactors. Appl Microbiol Biotech 97:3787–3800. https://doi.org/10.1007/s00253-013-4817-x
Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Biotechnol 19:138–144. https://doi.org/10.1016/j.copbio.2008.02.002
Gupta OP, Karkute SG, Banerjee S, Meena NL, Dahuja A (2017) Contemporary understanding of miRNA-based regulation of secondary metabolites biosynthesis in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00374
Häkkinen ST, Moyano E, Cusidó RM, Palazón J, Piñol MT, Oksman-Caldentey KM (2005) Enhanced secretion of tropane alkaloids in Nicotiana tabacum hairy roots expressing heterologous hyoscyamine-6b-hydroxylase. J Exp Bot 56:2611–2618. https://doi.org/10.1093/jxb/eri253
Hashimoto T, Yamada Y (2003) New genes in alkaloid metabolism and transport. Curr Opin Biotechnol 14:163–168. https://doi.org/10.1016/s0958-1669(03)00027-2
He J, Giusti MM (2010) Anthocyanins: natural colorants with health-promoting properties. Annu Rev Food Sci Technol 1:163–187. https://doi.org/10.1146/annurev.food.080708.100754
Herrera-Estrella L, Depicker A, Van Montague M, Schell J (1983) Expression of chimaeric genes transferred into plant cells using a ti-plasmid-derived vector. Nature 303:209–213. https://doi.org/10.1038/303209a0
Herrero M, Del Pilar Sánchez-Camargo A, Cifuentes A, Ibáñez E (2015) Plants, seaweeds, microalgae and food byproducts as natural sources of functional ingredients obtained using pressurized liquid extraction and supercritical fluid extraction. Trends Analyt Chem 71:26–38. https://doi.org/10.1016/j.trac.2015.01.018
Hidalgo D, Sanchez R, Lalaleo L, Bonfill M, Corchete P, Palazon J (2018) Biotechnological production of pharmaceuticals and biopharmaceuticals in plant cell and organ cultures. Curr Med Chem 25:3577–3596. https://doi.org/10.2174/0929867325666180309124317
Howles PA, Vincent JH, Sewalt V, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1994) Overexpression of i-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624. https://doi.org/10.1104/pp.112.4.1617
Hu L (2004) Production of shikonin by cell cultures of Lithospermum erythrorhizon. J Chin Med Mat 27:313–314
Huchelmann A, Boutry M, Hachez C (2017) Plant glandular trichomes: natural cell factories of high biotechnological interest. Plant Physiol 175:6–22. https://doi.org/10.1104/pp.17.00727
Hussain M, Fareed S, Ansari S, Rahman A, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4:10–20. https://doi.org/10.4103/0975-7406.92725
Ikeda T, Takashi Matsumoto T, Noguchi M (1977) Effects of inorganic nitrogen sources and physical factors on the formation of ubiquinone by tobacco plant cells in suspension culture. Agric Biol Chem 41:1197–1201. https://doi.org/10.1271/bbb1961.41.1197
Jarvis DE, Ho YS, Lightfoot DJ, Schmöckel SM, Li B, Borm TJA, Ohyanagi H, Mineta K, Michell CT, Saber N, Kharbatia NM, Rupper RR, Sharp AR, Dally N, Boughton BA, Woo YH, Gao G, Schijlen EGWM, Guo X, Momin AA, Negrão S, Al-Babili S, Gehring C, Roessner U, Jung C, Murphy K, Arold ST, Gojobori T, van der Linden CG, van Loo EN, Jellen EN, Maughan PJ, Tester M (2017) The genome of Chenopodium quinoa. Nature 542:307–312. https://doi.org/10.1038/nature21370
Jouhikainen K, Lindgren L, Jokelainen T, Hiltunen R, Teemu H, Teeri TH, Oksman-Caldentey KM (1999) Enhancement of scopolamine production in Hyoscyamus muticus L. hairy root cultures by genetic engineering. Planta 208:545–551. https://doi.org/10.1007/s004250050592
Khandare V, Walia S, Singh M, Kaur C (2011) Black carrot (Daucus carota ssp. sativus) juice: processing effects on antioxidant composition and color. FBP 89:482–486. https://doi.org/10.1016/j.fbp.2010.07.007
Kim S et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278
Knockaert M, Manigart S, Cattoird S, Verstraete W (2015) A perspective on the economic valorization of gene manipulated biotechnology: past and future. Biotechnol Rep 6:56–60. https://doi.org/10.1016/j.btre.2015.01.002
Kobayashi Y, Fukui H, Tabata M (1991) Effect of carbon dioxide and ethylene on berberine production and cell browning in Thalictrum minus cell cultures. Plant Cell Rep 9:496–499. https://doi.org/10.1007/bf00232104
Koca N, Karaman Ş (2015) The effects of plant growth regulators and l-phenylalanine on phenolic compounds of sweet basil. Food Chem 166:515–521. https://doi.org/10.1016/j.foodchem.2014.06.065
Kumar GS, Hazra S (2014) Sanguinarine, a promising anticancer therapeutic: photochemical and nucleic acid binding properties. RSC Adv 4:56518–56531. https://doi.org/10.1039/c4ra06456a
Laurila J, Laakso I, Valkonen JPT, Hiltunen R, Pehu E (1996) Formation of parental-type and novel glycoalkaloids in somatic hybrids between Solanum brevidens and S. tuberosum. Plant Sci 118:145–155. https://doi.org/10.1016/0168-9452(96)04435-4
Lee CH, Kim JH (2014) A review on the medicinal potentials of ginseng and ginsenosides on cardiovascular diseases. J. Ginseng Res 38:161–166. https://doi.org/10.1016/j.jgr.2014.03.001
Lee EK, Jin YW, Park JH, Yoo YM, Hong SM, Amir R, Yan Z, Kwon E, Elfick A, Tomlinson S, Halbritter F, Waibel T, Yun BW, Loake GJ (2010) Cultured cambial meristematic cells as a source of plant natural products. Nat Biotechnol 28:1213–1217. https://doi.org/10.1038/nbt.1693
Lee-Parsons CWT, Royce AJ (2006) Precursor limitations in methyl jasmonate-induced Catharanthus roseus cell cultures. Plant Cell Rep 25(6):607–612
Li R, Li R, Li X, Fu D, Zhu B, Tian H, Luo Y, Zhu H (2018) Multiplexed CRISPR/Cas9-mediated metabolic engineering of ϒ-aminobutyric acid levels in Solanum lycopersicum. Plant Biotechnol J 16:415–427. https://doi.org/10.1111/pbi.12781
Loyola-Vargas VM, Ochoa-Alejo N (2018) An introduction to plant tissue culture: advances and perspectives. Methods Mol Biol. https://doi.org/10.1007/978-1-4939-8594-4_1
Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC (2003) Virus-induced gene silencing in plants. Methods 30:296–303. https://doi.org/10.1016/s1046-2023(03)00037-9
Luque-Rodriguez JM, Perez-Juan P, De Castro MDL (2006) Extraction of polyphenols from vine shoots of Vitis vinifera by superheated ethanol-water mixtures. J Agric Food Chem 54:8775–8781. https://doi.org/10.1021/jf061855j
Marupudi NI, Han JE, Li KW, Renard VM, Tyler BM, Brem H (2007) Paclitaxel: a review of adverse toxicities and novel delivery strategies. Expert Opin Drug Saf 6:609–621. https://doi.org/10.1517/14740338.6.5.609
Mitsunaga Y, Takanaga H, Matsuo H, Naito M, Tsuruo T, Ohtani H, Sawada Y (2000) Effect of bioflavonoids on vincristine transport across blood–brain barrier. Eur J Pharmacol 395:193–201. https://doi.org/10.1016/s0014-2999(00)00180-1
Moon SH, Venkatesh J, Yu JW, Park SW (2015) Differential induction of meristematic stem cells of Catharanthus roseus and their characterization. Comptes Rendus Biol 338:745–756. https://doi.org/10.1016/j.crvi.2015.05.005
Moreira MM, Morais S, Barros AA, Delerue-Matos C, Guido LF (2012) A novel application of microwave-assisted extraction of polyphenols from brewer’s spent grain with HPLC-DAD-MS analysis. Anal Bioanal Chem 403:1019–1029. https://doi.org/10.1007/s00216-011-5703-y
Nair AJ, Sudhakaran PR, Rao JM, Ramakrishna SV (1992) Berberine synthesis by callus and cell suspension cultures of Coscinium fenestratum. Plant Cell Tissue Org Cult 29:7–10
Nakase I, Lai H, Singh NP, Sasaki T (2008) Anticancer properties of artemisinin derivatives and their targeted delivery by transferrin conjugation. Int J Pharm 354:28–33. https://doi.org/10.1016/j.ijpharm.2007.09.003
Ncube B, Van Staden J (2015) Tilting plant metabolism for improved metabolite biosynthesis and enhanced human benefit. Molecules 20:12698–12731. https://doi.org/10.3390/molecules200712698
Norman A, Aqeel M, Shuilin He S (2016) CRISPR–Cas9: tool for qualitative and quantitative plant genome editing. Front. Plant Sci 7:1740. https://doi.org/10.3389/fpls.2016.01740
Ochoa-Villarreal M, Howat S, Jang MO, Kim IS, Jin YW, Lee EK, Loake GJ (2015) Cambial meristematic cells: a platform for the production of plant natural products. New Biotechnol 32:581–587. https://doi.org/10.1016/j.nbt.2015.02.003
Ochoa-Villarreal M, Howat S, Hong S, Jang MO, Jin YW, Lee EK, Loake GJ (2016) Plant cell culture strategies for the production of natural products. BMB Rep 49:149–158. https://doi.org/10.5483/bmbrep.2016.49.3.264
Oksman-Caldentey KM, Inzé D (2004) Plant cell factories in the post-genomic era: new ways to produce designer secondary metabolites. Trends Plant Sci 9:433–440. https://doi.org/10.1016/j.tplants.2004.07.006
Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, Drake R (2005) Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol 23:482–487. https://doi.org/10.1038/nbt1082
Pennisi E (2016) The plant engineer. Science 353:1220–1224. https://doi.org/10.1126/science.353.6305.1220
Petolino JF (2015) Genome editing in plants via designed zinc finger nucleases. Vitro Cell Dev Biol Plant 51:1–8. https://doi.org/10.1007/s11627-015-9663-3
Prado JM, Vardanega R, Debien ICN et al (2015) Conventional Extraction. Food waste recovery processing technologies and industrial techniques. Academic Press imprint of Elsevier, Amsterdam, pp 127–148
Puri M, Sharma D, Barrow CJ (2012) Enzyme-assisted extraction of bioactives from plants. Trends Biotechnol 30:37–44. https://doi.org/10.1016/j.tibtech.2011.06.014
Rajkumpari S, Sanatombi K (2018) In Vitro production of some important secondary metabolites from zingiber species. Biotechnol Approaches Med Aromat Plants. https://doi.org/10.1007/978-981-13-0535-1_9
Ramegowda V, Mysore KS, Senthil-Kumar M (2014) Virus-induced gene silencing is a versatile tool for unraveling the functional relevance of multiple abiotic-stress-responsive genes in crop plants. Front Plant Sci. 8(5):323. https://doi.org/10.3389/fpls.2014.00323
Ramirez-Estrada K, Vidal-Limon H, Hidalgo D, Moyano E, Golenioswki M, Cusidó MR, Palazon J (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182. https://doi.org/10.3390/molecules21020182
Rao SR, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153. https://doi.org/10.1016/s0734-9750(02)00007-1
Rates SMK (2001) Plants as sources of drugs. Toxicon 39:603–613. https://doi.org/10.1016/S0041-0101(00)00154-9
Robins RJ, Rhodes MJC (1986) The stimulation of anthraquinone production by Cinchona ledyeriana cultures with polymeric adsorbents. Appl Microbiol Biotechnol 24:35–41. https://doi.org/10.1007/bf00266282
Rocha P, Stenzel O, Parr A, Walton N, Christou P, Drager B, Mark J, Leech MJ (2002) Functional expression of tropinone reductase I (trI) and hyoscyamine-6b-hydroxylase (h6h) from Hyoscyamus niger in Nicotiana tabacum. Plant Sci 162:905–913. https://doi.org/10.1016/s0168-9452(02)00033-x
Romagnoli LG, Knorr D (2009) Effects of ferulic acid treatment on growth and flavor development of cultured Vanilla planifolia cells. J Food Biotechnol 2:93–104. https://doi.org/10.1080/08905438809549678
Sadhukhan P, Saha S, Dutta S, Mahalanobish S, Sil PC (2018) Nutraceuticals: an emerging therapeutic approach against the pathogenesis of Alzheimer’s disease. Pharmacol Res 129:100–114. https://doi.org/10.1016/j.phrs.2017.11.028
Salgado-Garciglia R, Ochoa-Alcjo N (1990) Increased Capsaicin content in PFP-resistant cells of chili pepper (Capsicum annuum L.). Plant Cell Rep 8:617–620. https://doi.org/10.1007/bf00270067
Sánchez-Pujante PJ, Borja-Martínez M, Pedreño MÁ, Almagro L (2017) Biosynthesis and bioactivity of glucosinolates and their production in plant in vitro cultures. Planta 246:19–32. https://doi.org/10.1007/s00425-017-2705-9
Sasse F, Heckenberg U, Berlin J (1982) Accumulation of beta-carboline alkaloids and serotonin by cell cultures of Peganum harmala L: correlation between plants and cell cultures and influence of medium constituents. Plant Physiol 69:400–404. https://doi.org/10.1104/pp.69.2.400
Schachtsiek J, Warzecha H, Kayser O, Stehle F (2018) Current perspectives on biotechnological cannabinoid production in plants. Planta Med 84:214–220. https://doi.org/10.1055/s-0043-125087
Schiel O, Jarchow-Redecker K, Piehl GW, Lehmann J, Berlin J (1984) Increased formation of cinnamoyl putrescines by fedbatch fermentation of cell suspension cultures of Nicotiana tabacum. Plant Cell Rep 3:18–20. https://doi.org/10.1007/bf00270221
Segovia FJ, Luengo E, Corral-Pérez JJ, Raso J, Almajano MP (2015) Improvements in the aqueous extraction of polyphenols from borage (Borago officinalis L.) leaves by pulsed electric fields (PEF) applications. Ind Crops Prod 65:390–396. https://doi.org/10.1016/j.indcrop.2014.11.010
Sharma KD, Piqueras A (2010) Saffron (Crocus sativus L) tissue culture: micropropagation and secondary metabolite production. Funct Plant Sci Biotechnol 4:15–24
Smith RM (2003) Before the injection: modern methods of sample preparation for separation techniques. J Chromatogr A 1000:3–27. https://doi.org/10.1016/s0021-9673(03)00511-9
Solana M, Teel J, Hojilla-Evangelista M, Bertucco A, Eller F (2016) Counter-current carbon dioxide extraction of fat from soy skim. J Supercrit Fluids 113:106–111. https://doi.org/10.1016/j.supflu.2016.03.022
Steingroewer J, Bley T, Georgiev V, Ivanov I, Lenk F, Marchev A, Pavlov A (2013) Bioprocessing of differentiated plant in vitro systems. Eng Life Sci 13:26–38. https://doi.org/10.1002/elsc.201100226
Suhaj M (2006) Spice antioxidants isolation and their antiradical activity: a review. J Food Compos Anal 19(6–7):531–537. https://doi.org/10.1016/j.jfca.2004.11.005
Sun Y, Keli X, Yitao W, Xiuping C (2009) A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs. Anticancer Drugs 20:757–769. https://doi.org/10.1097/cad.0b013e328330d95b
Tatli I (2012) Plant cell tissue and organ culture in terpenoids. In: Biotechnological production of plant secondary metabolites. Bentham Science Publishers, Chapter 07, pp 107–123. https://doi.org/10.2174/978160805114411201010107
Tatsis EC, O’Connor SE (2016) New developments in engineering plant metabolic pathways. Curr Opin Biotechnol 42:126–132. https://doi.org/10.1016/j.copbio.2016.04.012
Tian L (2015) Using hairy roots for production of valuable plant secondary metabolites. Adv Biochem Eng Biotechnol 149:275–324. https://doi.org/10.1007/10_2014_298
Unver et al (2017) Genome of wild olive and the evolution of oil biosyhtesis. PNAS 114:E9413–E9422. https://doi.org/10.1073/pnas.1708621114 (Epub 2017 Oct 9)
Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297. https://doi.org/10.1126/science.289.5477.295
Veerport R, Contin A, Memelink J (2002) Biotechnology for the production of plant secondary metabolites. Phytochem Rev 1:13–25. https://doi.org/10.1023/a:1015871916833
Venugopala KN, Rashmi V, Odhav B (2013) Review on natural coumarin lead compounds for their pharmacological activity. BioMed Res Int. https://doi.org/10.1155/2013/963248 (ID 963248, 14 pages)
Verma P, Khan SA, Mathur AK, Ghosh S, Shanker K, Kalra A (2018) 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 251:1359–1371. https://doi.org/10.1007/s00709-014-0638-8
Verpoorte R, Memeling J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13:181–187. https://doi.org/10.1016/s0958-1669(02)00308-7
Wang L, Weller CL, Schlegel VL, Carr TP, Cuppett SL (2008) Supercritical CO2 extraction of lipids from grain sorghum dried distillers grains with solubles. Bioresour Technol 99:1373–1382. https://doi.org/10.1016/j.biortech.2007.01.055
Weathers PJ, Towler MJ, Xu J (2010) Bench to batch: advances in plant cell culture for producing useful products. Appl Microbiol Biotechnol 85:1339–1351. https://doi.org/10.1007/s00253-009-2354-4
White FF, Taylor BH, Huffman GA, Gordon MP, NesterE W (1985) Molecular and genetic analysis of the transferred DNA regions of the root-inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164:3–44
Wickremesinhe ERM, Arteca RN (1994) Taxus cell suspension cultures: optimizing growth and production of Taxol. J Plant Physiol 144(2):183–188
Wijesingh WAJP, Jeon YJ (2012) Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 283:6–12. https://doi.org/10.1016/j.fitote.2011.10.016
Wink M (2015) Modes of action of herbal medicines and plant secondary metabolites. Medicines (Basel) 2:251–286. https://doi.org/10.3390/medicines2030251
Yang T, Wang L, Zhu M, Zhang L, Yan L (2015) Properties and molecular mechanisms of resveratrol: a review. Pharmazie 70:501–506. https://doi.org/10.1691/ph.2015.5571
Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305. https://doi.org/10.1126/science.287.5451.303
Yun DJ, Hashimoto T, Yamada Y (1992) Metabolic engineering of medicinal plants: transgenic Atropa belladonna with an improved alkaloid composition. Proc Natl Acad Sci USA 89:11799–11803. https://doi.org/10.1073/pnas.89.24.11799
Zenk MH (1991) 6. Chasing the enzymes of secondary metabolism: plant cell cultures as a pot of gold. Phytochemistry 30(12):3861–3863
Zhang H, Hong Y, Huang L, Liu S, Tian L, Dai Y, Cao Z, Huang L, Li D, Song F (2016) Virus-induced gene silencing-based functional analyses revealed the involvement of several putative trehalose-6-phosphate synthase/phosphatase genes in disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 in Tomato. Front Plant Sci 7:1176. https://doi.org/10.3389/fpls.2016.01176
Zhao S, Baik OD, Choi YJ, Kim SM (2014) Pretreatments for the efficient extraction of bioactive compounds from plant-based biomaterials. Crit Rev Food Sci Nutr 54:1283–1297. https://doi.org/10.1080/10408398.2011.632698
Zhou P, Yang J, Zhu J, He S, Zhang W, Yu R, Zi J, Song L, Huang X (2015) Effects of β-cyclodextrin and methyl jasmonate on the production of vindoline, catharanthine, and ajmalicine in Catharanthus roseus cambial meristematic cell cultures. Appl Microbiol Biotechnol 99:7035–7045. https://doi.org/10.1007/s00253-015-6651-9
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Nielsen, E., Temporiti, M.E.E. & Cella, R. Improvement of phytochemical production by plant cells and organ culture and by genetic engineering. Plant Cell Rep 38, 1199–1215 (2019). https://doi.org/10.1007/s00299-019-02415-z
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DOI: https://doi.org/10.1007/s00299-019-02415-z