Metabolic Engineering of Plant Cellular Metabolism: Methodologies, Advances, and Future Directions

  • Rafael Zárate
  • Nabil el Jaber-Vazdekis
  • Robert Verpoorte
Chapter

Abstract

Plant natural products are useful compounds, such as pigments, fragrances, pharmaceuticals used for the treatment of several human diseases. Development of plant manipulation techniques, such as particle bombardment, Agrobacterium-mediated transformation, vacuum infiltration, agrodrench, viral vector, protoplasts fusion and ultrasound, as well as recombinant DNA, and genetic technologies applied toward metabolic engineering of bioactive plant natural products are presented, together with different genetic engineering methods, such as overexpression of transgenes, multiple expression of transgenes, gene silencing, and transcription factors as powerful tools for the engineering of biosynthetic pathways. Future perspectives and the potential of different approaches are presented to highlight how a better understanding of secondary metabolite pathways represents a direct successful highway to genetic manipulation of desired metabolic pathways.

Keywords

Hairy Root Metabolic Engineering Indole Alkaloid Tobacco Rattle Virus Vacuum Infiltration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors would like to thank Dr. Suman Chandra for the invitation to contribute to this book. RZ and NJV acknowledge Instituto Canario de Investigación del Cáncer and Agencia Canaria de Investigación Innovación y Sociedad de la Información, Spain for financial support.

References

  1. Abbadi A, Domergue F, Bauer J, Napier JA, Welti R, Zähringer U, Cirpus P, Heinz E (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constrains on their accumulation. Plant Cell 16:2734–2748PubMedGoogle Scholar
  2. Acereto-Escoffié POM, Chi-Manzanero BH, Echeverría-Echeverría S, Grijalva R, James Kay A, González-Estrada T, Castaño E, Rodríguez-Zapata LC (2005) Agrobacterium-mediated transformation of Musa acuminata cv. “Grand Nain” scalps by vacuum infiltration. Sci Horticult 105:359–371Google Scholar
  3. Aida R, Kishimoto S, Tanaka Y, Shibata M (2000a) Modification of flower color in torenia (Torenia fournieri Lind.) by genetic transformation. Plant Sci 153:33–42Google Scholar
  4. Aida R, Yoshida K, Kondo T, Kishimoto S, Shibata M (2000b) Copigmentation gives bluer flowers on transgenic torenia plants with the antisense dihydroflavonol-4-reductase gene. Plant Sci 160:49–56Google Scholar
  5. Allen RS, Millgate AG, Chitty JA, Thisleton J, Miller JAC, Fist AJ, Gerlach WL, Larkin PJ (2004) RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nat Biotechnol 22:1559–1566PubMedGoogle Scholar
  6. Barampura S, Zhang AJ (2011) Recent advances in plant transformation. Methods Mol Biol 701:1–35Google Scholar
  7. Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363Google Scholar
  8. Baulcombe DC (1999) Viruses and gene silencing in plants. Arch Virol Suppl 15:189–201PubMedGoogle Scholar
  9. Beaudoin F, Michaelson LV, Hey SJ, Lewis MJ, Shewry PR, Sayanova O, Napier JA (2000) Heterologous reconstitution in yeast of the polyunsaturated fatty acid biosynthetic pathway. Proc Natl Acad Sci USA 97:6421–6426PubMedGoogle Scholar
  10. Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Meth Mol Biol 82:259–266Google Scholar
  11. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2394PubMedGoogle Scholar
  12. Bovy A, de Vos R, Kemper M, Schijlen E, Almenar-Pertejo M, Muir S, Colllins 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 R1. Plant Cell 14:2509–2526PubMedGoogle Scholar
  13. Broun P (2004) Transcription factors as a tool for metabolic engineering in plants. Curr Op Plant Biol 7:202–209Google Scholar
  14. Browning LM (2003) n-3 polyunsaturated fatty acids, inflammation and obesity-related disease. Proc Nutr Soc 62:447–453PubMedGoogle Scholar
  15. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas PJJ (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14:3206–3214PubMedGoogle Scholar
  16. Cahoon EB, Kinney AJ (2005) The production of vegetable oils with novel properties: using genomic tools to probe and manipulate plant fatty acid metabolism. Eur J Lipid Sci Technol 107:239–243Google Scholar
  17. Campbell R, Ducreux LJ, Morris WL, Morris JA, Suttle JC, Ramsay G, Bryan GJ, Hedley PE, Taylor MA (2010) The metabolic and developmental roles of carotenoid cleavage dioxygenase 4 from potato. Plant Phisiol 154(2):656–664Google Scholar
  18. Cequier-Sánchez E, Rodríguez C, Dorta-Guerra R, Ravelo AG, Zárate R (2011) Echium acanthocarpum hairy root cultures, a suitable system for polyunsaturated fatty acid studies and production. BMC Biotechnol 11:42PubMedGoogle Scholar
  19. Chilton MD, Drummond MH, Merlo DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorogenesis. Cell 11:263–271PubMedGoogle Scholar
  20. Chintapakorn Y, Hamill JD (2003) 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 53:87–105PubMedGoogle Scholar
  21. Choi YH, van Spronsen J, Dai Y, Verberne M, Hollmann F, Arends IWCE, Witkamp GJ, Verpoorte R (2011) Are natural deep eutectic solvents the missing link in understanding cellular metabolism and physiology? Plant Physiol 156:1701–1705PubMedGoogle Scholar
  22. Christi Y (2003) Ultrasound the power of a silent gong. Biotechnol Adv 21:1Google Scholar
  23. Chung M-H, Chen M-K, Pan S-M (2000) Floral spray transformation can efficiently generate Arabidopsis transgenic plants. Transgen Res 9:471–476Google Scholar
  24. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedGoogle Scholar
  25. Cordero-Mesa M, Jiménez-Bermúdez S, Pliego-Alfaro F, Quesada MA, Mercado JA (2000) Agrobacterium cells as microprojectile coating: a novel approach to enhance stable transformation rates in strawberry. Aust J Plant Physiol 27:1093–1100Google Scholar
  26. Curtis IS (2005) Production of transgenic crops by the floral-dip method. Meth Mol Biol 286 (Transgenic Plants): 103–109Google Scholar
  27. Curtis IS, Nam HG (2001) Transgenic radish (Raphanus sativus L. longipinnatus Bailey) by floral-dip method - plant development and surfactant are important in optimizing transformation efficiency. Transgen Res 10:363–371Google Scholar
  28. Davey MR, Anthony P, Power BJ, Lowe KC (2005) Plant protoplasts: status and biotechnological perspectives. Biotechnol Adv 23:131–171PubMedGoogle Scholar
  29. Davies KM, Schwinn KE (2003) Transcriptional regulation of secondary metabolism. Funct Plant Biol 30:913–925Google Scholar
  30. de Majnik J, Weinman JJ, Djordjevic MA, Rolfe BG, Tanner GJ, Joseph RG, Larkin PJ (2000) Anthocyanin regulatory gene expression in transgenic white clover can result in an altered pattern of pigmentation. Aust J Plant Physiol 27:659–667Google Scholar
  31. DellaPenna D (2001) Plant metabolic engineering. Plant Physiol 125:160–163PubMedGoogle Scholar
  32. Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of Agrobacterium-mediated transformation by the Arabidopsis floral-dip method. Plant Physiol 123:895–904PubMedGoogle Scholar
  33. Dessaux Y, Petit A, Tempé J (1993) Chemistry and biochemistry of opines, chemical mediators of parasitism. Phytochemistry 34:31–38Google Scholar
  34. Dixon RA, Steele CL (2002) Flavonoids and isoflavonoids—a gold mine for metabolic engineering. Trends Plant Sci 4:394–400Google Scholar
  35. Dixon RA, Strack D (2003) Phytochemistry meets genome analysis, and beyond. Phytochemistry 62:815–816PubMedGoogle Scholar
  36. Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25:173–199PubMedGoogle Scholar
  37. Ducreux LJM, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MS (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of β-carotene and lutein. J Exp Bot 56:81–89PubMedGoogle Scholar
  38. Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27PubMedGoogle Scholar
  39. Fukusaki E, Kawasaki K, Kajiyama S, An C-I, Suzuki K, Tanaka Y, Kobayashi A (2004) Flower color modulations of Torenia hybrida by downregulation of chalcone synthase genes with RNA interference. J Biotechnol 111:229–240PubMedGoogle Scholar
  40. Goodrich J, Carpenter R, Coen ES (1992) A common gene regulates pigmentation pattern in diverse plant species. Cell 68:955–964PubMedGoogle Scholar
  41. Gronenborn B, Gardner RC, Schaefer S, Shepherd RJ (1981) Propagation of foreign DNA in plants using cauliflower mosaic virus as vector. Nature 294:773–776Google Scholar
  42. Grotewold E (2008) Transcription factors for predictive plant metabolic engineering: are we there yet? Curr Opin Biotechnol 10(2):138–144Google Scholar
  43. Hadi MZ, McMullen MD, Finner JJ (1996) Transformation of 12 different plasmids into soybean via particle bombardment. Plant Cell Rep 15:500–505Google Scholar
  44. Hain R, Bieseler B, Kindl H, Schroeder G, Stocker R (1990) Expression of a stilbene synthase gene in Nicotiana tabacum results in synthesis of the phytoalexin resveratrol. Plant Mol Biol 15:325–335PubMedGoogle Scholar
  45. Hallard DAC, van der Heijden R, Verpoorte R, Lopez-Cardoso I, Pasquali G, Memelink J, Hoge JHC (1997) Suspension cultured transgenic cells of Nicotiana tabacum expressing tryptophan decarboxylase and strictosidine synthase cDNAs from Catharanthus roseus produce strictosidine upon feeding of secologanin. Plant Cell Rep 17:50–54Google Scholar
  46. Hallard DAC, Palacios N, van der Heijden R, Memelink J, Verpoorte R (2000) Production of ajmalicine in transgenic Weigela styriaca tissue cultures expressing tdc and str cDNAs from Catharanthus roseus. Chapter 6. Transgenic plant cells for the production of indole alkaloids, Hallard DAC, PhD thesis, Leiden, University, pp 69–85Google Scholar
  47. Hansen G, Wright MS (1999) Recent advances in the transformation of plants. Trends Plant Sci 4:226–231PubMedGoogle Scholar
  48. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739PubMedGoogle Scholar
  49. Hooykaas PPJ (2000) Agrobacterium, a natural metabolic engineer of plants. In: Verpoorte R, Alfermann AW (eds) Metabolic Engineering of Plant Secondary Metabolism. Kluwer Academic Publishers, The NetherlandsGoogle Scholar
  50. Horrobin DF (1999) Lipid metabolism, human evolution and schizophrenia. Prostaglandins Leukot Essent Fatty Acids 60:431–437PubMedGoogle Scholar
  51. Hussain SS, Kayani MA, Amjad M (2011) Transcription factors as tools to engineer enhanced drought stress tolerance in plants. Biotechnology Prog 27(2):297–306Google Scholar
  52. Ingelbrecht I, Breyne P, Vancompernetlle K, Jacobs A, van Montagu M, Depicker A (1991) Transcriptional interference in transgenic plants. Gene 109:239–242PubMedGoogle Scholar
  53. Ishida Y, Saito H, Ohta S, Hiei Y, Komari T, Kumashiro T (1996) High frequency transformation of maize (Zea mays) mediated by Agrobacterium tumefaciens. Nat Biotechnol 14:745–750PubMedGoogle Scholar
  54. Iwase A, Matsui K, Ohme-Takagi M (2009) Manipulation of plant metabolic pathways by transcription factors. Plant Biotechnol 26:29–38Google Scholar
  55. Jacobs DI, Gaspari M, van der Greef J, van der Heijden R, Verpoorte R (2005) Proteome analysis of the medicinal plant Catharanthus roseus. Planta 221:690–704PubMedGoogle Scholar
  56. Jadhav A, Katavic V, Marillia EF, Giblin EM, Barton DL, Kumar A, Sonntag C, Babic V, Keller WA, Taylor DC (2005) Increased levels of erucic acid in Brassica carinata by co-suppression and antisense repression of the endogenous FAD2 gene. Metab Eng 7:215–220PubMedGoogle Scholar
  57. Jaworski J, Cahoon EB (2003) Industrial oils from transgenic plants. Curr Opin Plant Biol 6:178–184PubMedGoogle Scholar
  58. Joersbo M, Brunstedt J (1990) Direct gene transfer to plant protoplasts by mild sonication. Plant Cell Rep 9:207–210Google Scholar
  59. Kell DB (2004) Metabolomics and systems biology: making sense of the soup. Curr Opin Microbiol 7:296–307PubMedGoogle Scholar
  60. Klein TM, Wolf ED, Wu R, Sanford JC (1987) High-velocity microprojectiles for delivering nucleic acids into living cells. Nature 327:70–73Google Scholar
  61. Kristensen C, Morant M, Olsen CE, Ekstrom CT, Galbraith DW, Moller BL, Bak S (2005) Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. Proc Natl Acad Sci USA 102:1779–1784PubMedGoogle Scholar
  62. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V (2001) Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci USA 98:1871–1876PubMedGoogle Scholar
  63. Labra M, Vannini C, Grassi F, Bracale M, Balsemin M, Basso B, Sala F (2004) Genomic stability in Arabidopsis thaliana transgenic plants obtained by floral dip. Theor Appl Genet 109:1512–1518PubMedGoogle Scholar
  64. Leech MJ, Burtin D, Hallard D, Hillou F, Kemp B, Palacios N, Rocha P, O’Callaghan D, Verpoorte R, Christou P (2000) Particle gun methodology as a tool in metabolic engineering. In: Verpoorte R, Alfermann AW (eds) Metabolic Engineering of Plant Secondary Metabolism. Kluwer Academic Publishers, The NetherlandsGoogle Scholar
  65. Lessard PA, Kulaveerasingam H, York GM, Strong A, Sinskey AJ (2002) Manipulating gene expression for the metabolic engineering of plants. Metab Eng 4:67–79PubMedGoogle Scholar
  66. Lewinsohn E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam K-H, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S, Pichersky E (2001) Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256–1265PubMedGoogle Scholar
  67. Li J-F, Park E, von Arnim AG, Nebenführ A (2009) The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species. Plant Methods 5(6):1–15Google Scholar
  68. Liu Q, Singh S, Green A (2002) High-oleic and high-stearic cottonseed oils: nutritionally improved cooking oils developed using gene silencing. J Am Coll Nutr 21:205S–211SPubMedGoogle Scholar
  69. Liu Y, Yang H, Sakanishi A (2005) Ultrasound: mechanical gene transfer into plant cells by sonoporation. Biotechnol Adv 24(1):1–16PubMedGoogle Scholar
  70. Lorence A, Verpoorte R (2004) Gene transfer and expression in plants. In: Balbás P, Lorence A (eds) Methods in Molecular Biology, Recombinant Gene Expression. Reviews and Protocols. Humana Press Inc, TotowaGoogle Scholar
  71. McGinnis KM (2010) RNAi for functional genomics in plants. Brief Funct Genomics 9(2):111–117PubMedGoogle Scholar
  72. Melchers LS, Regensburg-Tuink AJG, Schilperoort RA, Hooykaas PJJ (1989) Specificity of signal molecules on the activation of Agrobacterium virulence gene expression. Mol Microbiol 3:969–977PubMedGoogle Scholar
  73. Memelink J, Kijne JW, van der Heijden R, Verpoorte R (2001a) Genetic modification of plant secondary metabolite pathways using transcriptional regulators. Adv Biochem Engineering/Biotechnol 72:103–125Google Scholar
  74. Memelink J, Verpoorte R, Kijne JW (2001b) ORCAnisation of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219PubMedGoogle Scholar
  75. Michielse CB, Hooykaas PJ, Van der Hondel CA, Ram AF (2005) Agrobacterium-mediated transformation as a tool for functional genomics in fungi. Curr Genetics 48:1–17Google Scholar
  76. Mohanpuria P, Kumar V, Ahuja PS, Yadav SK (2010) Agrobacterium-Mediated Silencing of Caffeine Synthesis through Root Transformation in Camellia sinensis L. Mol Biotechnol doi: 10.1007/s12033-010-9364-4 Google Scholar
  77. Moisyadi S, Neupane KR, Stiles JI (1998) Cloning and characterization of a cDNA encoding xanthosine-N7-methyltransferase from coffee (Coffea arabica). Acta Horticult 461:367–377Google Scholar
  78. Montiel G, Breton C, Doireau P, Jay-Allemand C, Gantet P (2003) Transcription factors that regulate secondary metabolism biosynthesis pathways: key actors for plant eco-physiology and ontogeny. Rec Res Devel Plant Cell Physiol 1:83–98Google Scholar
  79. Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, de Vos CHR, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruits containing increased levels of flavonols. Nat Biotechnol 19:470–474PubMedGoogle Scholar
  80. Napier JA, Sayanova O, Qi B, Lazarus CM (2004) Progress toward the production of long-chain polyunsaturated fatty acids in transgenic plants. Lipids 39:1067–1075PubMedGoogle Scholar
  81. Naqvi S, Farré G, Sanahuja G, Capell T, Zhu C, Christou P (2010) When more is better: multigene engineering in plants. Trends Plant Sci 15(1):48–56PubMedGoogle Scholar
  82. Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis thaliana. Plant Cell 12:1863–1878PubMedGoogle Scholar
  83. Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114PubMedGoogle Scholar
  84. O’Brien J, Lummis SCR (2004) Biolistic and diolistic transfection: using the gene gun to deliver DNA and lipophilic dyes into mammalian cells. Methods 33:121–125PubMedGoogle Scholar
  85. Ogita S, Uefuji H, Morimoto M, Sano H (2004) Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol Biol 54:931–941PubMedGoogle Scholar
  86. Ogita S, Uefuji H, Yamaguchi Y, Koizumi N, Sano H (2003) RNA interference: producing decaffeinated coffee plants. Nature 423:823PubMedGoogle Scholar
  87. Oksman-Caldentey K-M, Barz WH (2002) Plant Biotechnology and Transgenic Plants. In: Oksman-Caldentey K-M, Barz WH (ed) C.H.I.P.S. Texas, USAGoogle Scholar
  88. Oksman-Caldentey K-M, Inzé D, Oresic M (2004) Connecting genes to metabolites by a systems biology approach. Proc Natl Acad Sci USA 101:9949–9950PubMedGoogle Scholar
  89. Oliver DJ, Nikolau B, Syrkin-Wurtele E (2002) Functional genomics: high throughput mRNA, protein and metabolite analyses. Metab Eng 4:98–106PubMedGoogle Scholar
  90. Olmedo-Monfil V, Cortes-Penagos C, Herrera-Estrella A (2004) Three decades of fungal transformation: key concepts and applications. Meth Mol Biol 267:297–313Google Scholar
  91. Page JE (2005) Silencing nature′s narcotics: metabolic engineering of the opium poppy. Trends Biotechnol 23:331–333PubMedGoogle Scholar
  92. Pomahacová B, Dusek J, Dusková J, Yazaki K, Roytrakul S, Verpoorte R (2009) Improved accumulation of ajmalicine and tetrahydroalstonine in Catharanthus cells expressing an ABC transporter. J Plant Physiol 166:1405–1412PubMedGoogle Scholar
  93. Porta C, Lomonossoff GP (2002) Viruses as vectors for the expression of foreign sequences in plants. Biotechnol Gen Eng Rev 19:245–291Google Scholar
  94. Potrykus I (1991) Gene transfer to plants: assessment of published approaches and results. Annu Rev Plant Physiol Plant Mol Biol 42:205–225Google Scholar
  95. Qi B, Fraser T, Mugford S, Dobson G, Sayanova O, Butler J, Napier JA, Stobart AK, Lazarus CM (2004) The production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in transgenic plants. Nat Biotechnol 22:739–745PubMedGoogle Scholar
  96. Quattrocchio F, Wing J, van der Woude K, Mol JN, Koes R (1998) Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J 13:475–488PubMedGoogle Scholar
  97. Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol JN, Koes R (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444PubMedGoogle Scholar
  98. Rodríguez-Talou J, Verbene MC, Budi Muljono RA, van Tegelen LJP, Gonsalvez-Bernal B, Linthorst HJM, Wullems GJ, Bol JF, Verpoorte R (2001) Isochorismate synthase transgenic expression in Catharanthus roseus cell suspensions. Plant Physiol Biochem 39:595–602Google Scholar
  99. Roytrakul S, Verpoorte R (2007) Role of vacuolar transporter proteins in plant secondary metabolism: Catharanthus roseus cell culture. Phytochemistry Rev 6:383–396Google Scholar
  100. Ryu C-M, Anand A, Kang L, Mysore KS (2004) Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse Solanaceous species. Plant J 40:322–331PubMedGoogle Scholar
  101. Sanford JC (1988) The biolistic process. Trends Biotechnol 6:299–302Google Scholar
  102. Sanford JC, Klein TM, Wolf ED, Allen N (1987) Delivery of substances into cells and tissue using a particle bombardment process. Trends Biotechnol 6:299–302Google Scholar
  103. Sauret-Güeto S, Botella-Pavia P, Rodríguez-Concepción M (2003) Molecular tools for the metabolic engineering of carotenoids biosynthesis in plants. Recent Res Devel Plant Mol Biol 1:339–363Google Scholar
  104. Sayanova OV, Napier JA (2004) Eicosapentaenoic acid: biosynthetic routes and the potential for synthesis in transgenic plants. Phytochemistry 65:147–158PubMedGoogle Scholar
  105. Sayanova OV, Smith MA, Lapinskas P, Stobart AK, Dobson G, Christie WW, Shewry PR, Napier JA (1997) Expression of a borage cDNA containing an N-terminal cytochrome b5 domain results in the accumulation of high levels of Δ6-desaturated fatty acids in transgenic tobacco. Proc Natl Acad Sci USA 94:4211–4216PubMedGoogle Scholar
  106. Senthil-Kumar M, Mysore KS (2011) Virus-induced gene silencing can persist for more than 2 years and also be transmitted to progeny seedlings in Nicotiana benthamiana and tomato. Plant Biotechnol J 9:797–806PubMedGoogle Scholar
  107. Sharp PA (2001) RNA interference. Genes Dev 15:485–490PubMedGoogle Scholar
  108. Shikata M, Ohme-Takagi M (2008) The utility of transcription factors for manipulation of floral traits. Plant Biotechnol 25:31–36Google Scholar
  109. Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K (2003) Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc Natl Acad Sci USA 100:751–756PubMedGoogle Scholar
  110. Shrawat AK, Good AG (2011) Agrobacterium tumefaciens-mediated genetic transformation of cereals using immature embryos. Methods Mol Biol 710:355–372PubMedGoogle Scholar
  111. Simonopoulus AP (1991) Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr 54:438–463Google Scholar
  112. Simonsen S, van’t Veer P, Strain JJ (1998) Adipose tissue omega-3 and omega-6 fatty acid content and breast cancer in the EURAMIC study. Am J Epidemiol 147:342–352PubMedGoogle Scholar
  113. Sinha A, Wetten AC, Caligari PDS (2003) Effect of biotic factors on the isolation of Lupinus albus protoplasts. Aust J Bot 51:103–109Google Scholar
  114. Sinkar VP, White FF, Gordon MP (1987) Molecular biology of Ri-plasmid. A rev J Biosci 11:47–57Google Scholar
  115. Smith FD, Harpending PR, Sanford JC (1992) Biolistic transformation of prokaryotes: factors that affect biolistic transformation of very small cells. J Gen Microbiol 138:239–248PubMedGoogle Scholar
  116. St-Pierre B, Vazquez-Flota F, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:887–900PubMedGoogle Scholar
  117. Tang W (2003) Additional virulence genes and sonication enhance Agrobacterium tumefaciens-mediated loblolly pine transformation. Plant Cell Rep 21:555–562PubMedGoogle Scholar
  118. Tattersall DB, Bak S, Jones PR, Olsen CE, Nielsen JK, Hansen ML, Hoj PB, Moller BL (2001) Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science 293:1826–1828PubMedGoogle Scholar
  119. Tepfter D (1990) Genetic transformation using Agrobacterium rhizogenes. Physiol Plant 79:140–146Google Scholar
  120. Thelen JJ, Ohlorgge JB (2002) Metabolic engineering of fatty acid biosynthesis in plants. Metab Eng 4:12–21PubMedGoogle Scholar
  121. Trautwein EA (2001) n-3 Fatty acids–physiological and technical aspects for their use in food. Eur J Lipid Sci Technol 103:45–55Google Scholar
  122. Trethewey RN (2004) Metabolite profiling as an aid to metabolic engineering in plants. Curr Opin Plant Biol 7:196–201PubMedGoogle Scholar
  123. Trick HR, Finner JJ (1997) SAAT: sonication-assisted Agrobacterium-mediated transformation. Transgen Res 6:329–336Google Scholar
  124. Ueki S, Lacroix B, Krichevsky A, Lazarowitz SG, Citovsky V (2009) Functional transient genetic transformation of Arabidopsis leaves by biolistic bombardment. Nat Protoc 4(1):71–77PubMedGoogle Scholar
  125. Ursin VA (2003) Modification of plant lipids for human health: development of functional land-based omega-3 fatty acids. Symposium: improving human nutrition through genomics, proteomics and biotechnologies. American Society Nutrition science, pp 4271–4276Google Scholar
  126. Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297PubMedGoogle Scholar
  127. Van der Heijden R, Jacobs DI, Snoeijer W, Hallard D, Verpoorte R (2004) The Catharanthus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11:1241–1253Google Scholar
  128. Van der Krol AR, Lenting PE, Veenstra J, Van der Meer IM, Koes RE, Gerats AGM, Mol JNM, Stuitje AR (1988) An anti-sense chalcone synthase gene in transgenic plants inhibits flower pigmentation. Nature 333:866–869Google Scholar
  129. Verberne M, Verpoorte R, Bol J, Mercado-Blanco J, Linthorst HJM (2000) Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nat Biotechnol 18:779–783PubMedGoogle Scholar
  130. Verpoorte R, Alfermann AW (2000) Metabolic engineering of plant secondary metabolism. In: Verpoorte R, Alfermann AW (ed) Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  131. Verpoorte R, van der Heijden R, Memelink J (2000) Engineering the plant cell factory for secondary metabolite production. Transgen Res 9:323–343Google Scholar
  132. Verpoorte R, van der Heijden R, Ten Hoopen HJG, Memelink J (1999) Metabolic engineering of plant secondary metabolite pathways from the production of fine chemicals. Biotechnol Lett 21:467–479Google Scholar
  133. Vom Endt D, Kijne JW, Memelink J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators? Phytochemistry 61:107–114PubMedGoogle Scholar
  134. Wang TT, Choi YJ, Lee BH (2001) Transformation systems of non-Saccharomyces yeasts. Crit Rev Biotechnol 21:177–218PubMedGoogle Scholar
  135. Waterhouse PM, Wang M, Finnegan EJ (2001a) Role of short RNAs in gene silencing. Trends Plant Sci 6:297–301Google Scholar
  136. Waterhouse PM, Wang M, Lough T (2001b) Gene silencing as an adaptive defence against viruses. Nature 411:834–842Google Scholar
  137. Weber S, Friedt W, Landes N, Molinier J, Himber C, Rousselin P, Hahne G, Horn R (2003) Improved Agrobacterium-mediated transformation of sunflower (Helianthus annuus L.): assessment of macerating enzymes and sonication. Plant Cell Rep 21:475–482PubMedGoogle Scholar
  138. Whitmer S, Canel C, Hallard D, Goncalves C, Verpoorte R (1998) Influence of precursor availability on alkaloid accumulation by transgenic cell lines of Catharanthus roseus. Plant Physiol 116:853–857PubMedGoogle Scholar
  139. Whitmer S, Canel C, van der Heijden R, Verpoorte R (2003) Long-term instability of alkaloid production by stably transformed cell lines of Catharanthus roseus. Plant Cell Tiss Org Cult 74:73–80Google Scholar
  140. Whitmer S, van der Heijden R, Verpoorte R (2002a) Effect of precursor feeding on alkaloid accumulation by a tryptophan decarboxylase overexpressing transgenic cell line T22 of Catharanthus roseus. J Biotechnol 96:193–203Google Scholar
  141. Whitmer S, van der Heijden R, Verpoorte R (2002b) Effect of precursor feeding on alkaloid accumulation by a strictosidine synthase over-expressing transgenic cell line S1 of Catharanthus roseus. Plant Cell Tiss Org Cult 69:85–93Google Scholar
  142. Whitmer S, van der Heijden R, Verpoorte R (2002c) Genetic engineering of the plant cell factory for secondary metabolite production. Indole Alkaloid production in Catharanthus roseus as a model. In: Oksman-Caldentey K-M, Barz WH (ed) Plant biotechnology and transgenic plants. Scitech publishing, New YorkGoogle Scholar
  143. Wilson TMA, Davies JW (1992) Genetic engineering with plant viruses. CRC Press, Boca Raton, FloridaGoogle Scholar
  144. Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307PubMedGoogle Scholar
  145. Ye GN, Stone D, Pang SZ, Creely W, Gonzalez K, Hinchee M (1999) Arabidopsis ovule is the target for Agrobacterium in planta vacuum infiltration transformation. Plant J 19:249–257PubMedGoogle Scholar
  146. Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid free) rice endosperm. Science 287:303–305PubMedGoogle Scholar
  147. 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 89:11799–11803PubMedGoogle Scholar
  148. Zambre M, Terryn N, de Clercq J, de Buck S, Dillen W, van Montagu M, van der Straeten D, Angenon G (2003) Light strongly promotes gene transfer from Agrobacterium tumefaciens to plant cells. Planta 216:580–586PubMedGoogle Scholar
  149. Zárate R (2010) Plant secondary metabolism engineering: methods, strategies, advances, and omics. In. Mander L, Lui H-W (ed) Comprehensive natural products II chemistry and biology, vol. 3. Elsevier, Oxford, pp 629–668Google Scholar
  150. Zárate R, Dirks C, van der Heijden R, Verpoorte R (2001) Terpenoid indole alkaloid profile changes in Catharanthus pusillus during development. Plant Sci 160:971–977PubMedGoogle Scholar
  151. Zárate R, Verpoorte R (2007) Strategies for the genetic modification of the medicinal plant Catharanthus roseus (L.) G. Phytochem Rev 6(2–3):475–491Google Scholar
  152. Zárate R, Yeoman MM (2001) Application of recombinant DNA technology to studies on plant secondary metabolism. In: Bender L, Kumar A (eds) From Soil to Cell—A Broach Approach to Plant Life. Giessen Electronic Library, GermanyGoogle Scholar
  153. Zhang W, Curtin C, Franco C (2002) Towards manipulation of post-biosynthetic events in secondary metabolism of plant cell cultures. Enzyme Microbiol Technol 30:688–696Google Scholar
  154. Zhou X, Wei Y, Zhu H, Wang Z, Lin J, Liu L, Tang K (2008) Protoplast formation, regeneration and transformation from the taxol-producing fungus Ozonium sp. African J Biotechnol 7(12):2017–2024Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Rafael Zárate
    • 1
  • Nabil el Jaber-Vazdekis
    • 1
  • Robert Verpoorte
    • 2
  1. 1.Instituto Canario de Investigación del Cáncer, Hospital Universitario La CandelariaSanta Cruz de TenerifeSpain
  2. 2.Natural Products LaboratoryInstitute of Biology Leiden, University of LeidenLeidenThe Netherlands

Personalised recommendations