Advertisement

Handling Dangerous Molecules: Transport and Compartmentation of Plant Natural Products

  • Markus Klein
  • Werner Roos
Chapter

Abstract

The plant cell faces a dilemma: secondary products provide a multitude of defence and signalling functions, but their biosynthesis poses a severe burden, as it competes for energy sources and building blocks and may generate toxic products. Thus, evolution of recent secondary metabolites is not only driven by their advantageous functions but also selects for strict control mechanisms including the integration of biosynthesis into the cellular ultrastructure. In order to minimize the risk of self-intoxication, secondary products are usually targeted into compartments of low metabolic activity, notably the vacuole and the extracellular space. This is most obvious for phenolic substances but also for alkaloids, the best studied plant toxins. Compartmentation on a cellular or subcellular level is also instrumental in plants synthesizing preformed defence substances such as cyanogenic glycosides in order to assure that the active toxins are only liberated in case of an attack. Biosynthetic pathways and regulatory elements are well-established at least for some natural compound classes such as the flavonoids. In contrast, our knowledge of transport steps behind the subcellular distribution of these substances is just scratching the surface.

This chapter provides an overview on transport processes involved in secondary metabolite compartmentation that is concentrated at the best known areas of flavonoid and alkaloid production. Starting from ‘classical’ data of secondary metabolite transport we characterize the actually known transporters – which mainly belong to the ATP-Binding Cassette (ABC) or Multidrug and Toxic Extrusion (MATE) superfamilies – and their specific functioning in cells and tissues as analyzed by modern experimental techniques. The ‘transporter’ hypothesis is confronted with ‘vesicle transport’ models of subcellular trafficking. Although it appears premature to find common ground between these alternative models, the discovery of novel cellular functions of secondary metabolites facilitates our understanding of an intimate interplay between biosynthetic steps, transmembrane fluxes and metabolic channels, i.e. the plant’s solution to the ‘toxic dilemma’.

Keywords

Biosynthetic Enzyme Alkaloid Biosynthesis Berberine Bridge Enzyme Vacuolar Lumen Black Mexican Sweet 
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

Acknowledgements

Work in the former lab of MK was supported by the Swiss National Science Foundation. MK wishes to thank his former team, especially E. Martinoia, B. Weder, K. Marinova, C. Ballmann, K. Schmid, A. Polinceusz, H. Grob, B. Burla and T. Kretschmar (all Univ. of Zurich). MK acknowledges Daniel Studer, University of Bern, for his experimental help to obtain Fig. 3. Work in the lab of WR was supported by the Deutsche Forschungsgemeinschaft and the Excellence Cluster Sachsen-Anhalt. WR gratefully acknowledges contributions of D. Weiss, K. Färber, K. Viehweger, M. Heinze, M. Hieke, G. Danders and K. Thomasch.

References

  1. Abrahams S, Lee E, Walker AR, Tanner GJ, et al (2003) The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant J 35:624–636PubMedGoogle Scholar
  2. Achnine L, Blancaflor EB, Rasmussen S, et al (2004) Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16:3098–3109PubMedGoogle Scholar
  3. Alcantara J, Bird DA, Franceschi VR, et al (2005) Sanguinarine biosynthesis is associated with the endoplasmic reticulum in cultured opium poppy cells after elicitor treatment. Plant Physiol 138:173–183PubMedGoogle Scholar
  4. Alfenito MR, Souer E, Goodman CD, et al (1998) Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 10:1135–1149PubMedGoogle Scholar
  5. Allen RS, Miller JAC, Chitty JA, et al (2008) Metabolic engineering of morphinan alkaloids by over-expression and RNAi suppression of salutaridinol7-O-acetyltransferase in opium poppy. Plant Biotech J 6:22–30Google Scholar
  6. Allen RS, Millgate AG, Chitty JA, et al (2004) RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nature Biotech 22:1559–1568Google Scholar
  7. Amann M, Wanner G, Zenk MH (1986) Intracellular compartmentation of two enzymes of berberine biosynthesis in plant cell cultures. Planta 167:310–320Google Scholar
  8. Anhalt S, Weissenböck G (1992) Subcellular localization of luteolin glucuronides and related enzymes in rye mesophyll. Planta 187:83–88Google Scholar
  9. Apse MP, Aharon GS, Snedden WA, et al (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedGoogle Scholar
  10. Arakawa H, Clark WG, Psenak M, et al (1992) Purification and characterization of dihydro­benzophenanthridine oxidase from elicited Sanguinaria canadensis cell cultures. Arch Biochem Biophys 299:1–7PubMedGoogle Scholar
  11. Badri DV, Loyola-Vargas VM, Broeckling CD, et al (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-Binding Cassette (ABC) transporter mutants. Plant Physiol 146:762–771PubMedGoogle Scholar
  12. Bais HP, Park SW, Weir TL, et al (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32PubMedGoogle Scholar
  13. Bajaj NP, McLean MJ, Waring MJ, et al (1990) Sequence-selective, pH-dependent binding to DNA of benzophenanthridine alkaloids. J Mol Recognit 3:48–54PubMedGoogle Scholar
  14. Bartak P, Simanek V, Vlckova M, et al (2003) Interactions of sanguinarine and chelerythrine with molecules containing a mercapto group. J Phys Org Chem 16:803–810Google Scholar
  15. Bartholomew DM, Van Dyk DE, Lau S-MC, et al (2002) Alternate energy-dependent pathways for the vacuolar uptake of glucose and glutathione conjugates. Plant Physiol 130:1562–1572PubMedGoogle Scholar
  16. Barz W, Mackenbrock U (1994) Constitutive and elicitation induced metabolism of isoflavones and pterocarpans in chickpea (Cicer arietinum) cell suspension cultures. Plant Cell, Tissue Organ Culture 38:199–211Google Scholar
  17. Baxter IR, Young JC, Armstrong G, et al (2005) A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proc Natl Acad Sci USA 102:2649–2654PubMedGoogle Scholar
  18. Bird DA, Facchini PJ (2001) Berberine bridge enzyme, a key branch-point enzyme in benzylisoquinoline alkaloid biosynthesis, contains a vacuolar sorting determinant. Planta 213:888–897PubMedGoogle Scholar
  19. Bird D, Beisson F, Brigham A, et al (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52:485–498PubMedGoogle Scholar
  20. Birnbaum K, Shasha DE, Wang JY, et al (2003) A gene expression map of the Arabidopsis root. Science 302:1956–1960PubMedGoogle Scholar
  21. Blom TJM, Sierra M, van Vliet TB, et al (1991) Uptake and accumulation of ajmalicine into isolated vacuoles of cultured cells of Catharanthus roseus (L.) G. Don. and its conversion into serpentine. Planta 183:170–177Google Scholar
  22. Blume DE, Jaworski JG, McClure JW (1979) Uridinediphosphate-glucose: Isovitexin 7-O-glucosyltransferase from barley protoplasts: Subcellular localization. Planta 146:199–202Google Scholar
  23. Bock A, Wanner G, Zenk MH (2002) Immunocytological localization of two enzymes involved in berberine biosynthesis. Planta 216:57–63PubMedGoogle Scholar
  24. Braun R, Keller F (2000) Vacuolar chain elongation of raffinose oligosaccharides in Ajuga reptans. Funct Plant Biol 27:743–746Google Scholar
  25. Brouillard R, Dangles O (1994) Flavonoids and flower colour. In: H Harbord, JB Harborne, eds, The flavonoids: advances in research since 1986. CRC Press, Boca Raton, FL, pp 565–588Google Scholar
  26. Brown MH, Paulsen IT, Skurray RA (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:394–395PubMedGoogle Scholar
  27. Brown DE, Rashotte AM, Murphy AS, et al (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535PubMedGoogle Scholar
  28. Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145:478–490PubMedGoogle Scholar
  29. Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191–1205PubMedGoogle Scholar
  30. Burchard P, Bilger W, Weissenböck G (2000) Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant Cell Environ 23:1373–1380Google Scholar
  31. Burlat V, Oudin A, Courtois M, et al (2004) Co-expression of three MEP pathway genes and geraniol 10-hydroxylase in internal phloem parenchyma of Catharanthus roseus implicates multicellular translocation of intermediates during the biosynthesis of monoterpene indole alkaloids and isoprenoid-derived primary metabolites. Plant J 38:131–141PubMedGoogle Scholar
  32. Chong J, Baltz R, Schmitt C, et al (2002) Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin glucoside accumulation, enhances oxidative stress, and weakens virus resistance. Plant Cell 14:1093–1107PubMedGoogle Scholar
  33. Chou WM., Kutchan TM (1998) Enzymatic oxidations in the biosynthesis of complex alkaloids. Plant J 15:289–300PubMedGoogle Scholar
  34. Cline SD, Coscia CJ (1989) Ultrastructural changes associated with the accumulation and secretion of sanguinarine in Papaver bracteatum suspension cultures treated with fungal elicitor. Planta 178:303–314Google Scholar
  35. Cole SP, Bhardwaj G, Gerlach JH, et al (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650–1654PubMedGoogle Scholar
  36. Cole SPC, Deeley RG (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 27:438–446PubMedGoogle Scholar
  37. Collins NC, Thordal-Christensen H, Lipka V, et al (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973–977PubMedGoogle Scholar
  38. Conn S, Zhang W, Franco C (2003) Anthocyanic vacuolar inclusions (AVIs) selectively bind acylated anthocyanins in Vitis vinifera L. (grapevine) suspension culture. Biotechnol Lett 25:835–839PubMedGoogle Scholar
  39. Costet L, Fritig B, Kauffmann S (2002) Scopoletin expression in elicitor-treated and tobacco mosaic virus-infected tobacco plants. Physiol Plant 115:228–235PubMedGoogle Scholar
  40. De Luca, V. (1993) Indole alkaloid biosynthesis. In: Lea, P., ed, Methods in plant biochemistry. Enzymes of secondary metabolism, Vol. 9, pp 345–368, Academic PressGoogle Scholar
  41. De Luca V, St-Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 4:168–173Google Scholar
  42. De Luca V, Cutler AJ (1987) Subcellular localization of enzymes involved in indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 85:1099–1102PubMedGoogle Scholar
  43. Dean JV, Devarenne TP (1997) Peroxidase-mediated conjugation of glutathione to unsaturated phenylpropanoids. Evidence against glutathione S-transferase involvement. Physiol Plant 99:271–278Google Scholar
  44. Dean JV, Devarenne TP, Lee IS, et al (1995) Properties of a maize glutathione S-transferase that conjugates coumaric acid and other phenylpropanoids. Plant Physiol 108:985–994PubMedGoogle Scholar
  45. Dean JV, Mills JD (2004) Uptake of salicylic acid 2-O-ß-D-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol Plant 120:603–612PubMedGoogle Scholar
  46. Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, et al (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13:853–871PubMedGoogle Scholar
  47. Debeaujon I, Nesi N, Perez P, et al (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15:2514–2531PubMedGoogle Scholar
  48. Deeley RG, Cole SPC (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 580:1103–1111PubMedGoogle Scholar
  49. Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, et al (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730PubMedGoogle Scholar
  50. Deus-Neumann B, Zenk MH (1984) A highly selective alkaloid uptake system in vacuoles of higher plants. Planta 162:250–260Google Scholar
  51. Deus-Neumann B, Zenk MH (1986) Accumulation of alkaloids in plant vacuoles does not involve an ion-trap mechanism. Planta 167:44–53Google Scholar
  52. Diener AC, Gaxiola RA, Fink GR (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. Plant Cell 13:1625–1638PubMedGoogle Scholar
  53. Drose S, Altendorf K (1997) Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200:1–8PubMedGoogle Scholar
  54. Dudler R, Hertig C (1992) Structure of an Mdr-like gene from Arabidopsis thaliana - Evolutionary implications. J Biol Chem 267:5882–5888PubMedGoogle Scholar
  55. Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205PubMedGoogle Scholar
  56. Ehlting J, Mattheus N, Aeschliman DS, et al (2005) Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J 42:618–640PubMedGoogle Scholar
  57. Facchini PJ, Bird DA (1998) Developmental regulation of benzylisoquinoline alkaloid biosynthesis in opium poppy plants and tissue cultures. In Vitro Cellular and Developmental Biology Plant 34:69–79.Google Scholar
  58. Facchini PJ, St-Pierre B (2005) Synthesis and trafficking of alkaloid biosynthetic enzymes. Curr Opin Plant Biol 8:657–666PubMedGoogle Scholar
  59. Facchini PF (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Physiol Plant Mol Biol 52:29–66PubMedGoogle Scholar
  60. Faddeeva MD, Beliaeva TN (1997) Sanguinarine and ellipticine cytotoxic alkaloids isolated from well-known antitumor plants. Intracellular targets of their action. Tsitologiia 39:181–208PubMedGoogle Scholar
  61. Färber K, Schumann B, Miersch O, et al (2003) Selective desensitization of jasmonate- and pH-dependent signaling in the induction of benzophenanthridine biosynthesis in cells of Eschscholzia californica. Phytochemistry 62:491–500PubMedGoogle Scholar
  62. Forestier C, Frangne N, Eggmann T, et al (2003) Differential sensitivity of plant and yeast MRP (ABCC)-mediated organic anion transport processes towards sulfonylureas. FEBS Lett 554:23–29PubMedGoogle Scholar
  63. Frangne N, Eggmann T, Koblischke C, et al (2002) Flavone glucoside uptake into barley mesophyll and Arabidopsis cell culture vacuoles. Energization occurs by H+-antiport and ATP-binding cassette-type mechanisms. Plant Physiol 128:726–733PubMedGoogle Scholar
  64. Frehner M, Keller F, Wiemken A (1984) Localization of fructan metabolism in the vacuoles isolated from protoplasts of Jerusalem artichoke tubers (Helianthus tuberosus L.). J Plant Physiol. 116:197–208Google Scholar
  65. Galneder E, Rueffer M, Wanner G, et al (1988) Alternative final steps in berberine biosynthesis in Coptis japonica cell cultures. Plant Cell Rep 7:1–4Google Scholar
  66. Gao XQ, Li CG, Wei PC, et al (2005) The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiol 139:1207–1216PubMedGoogle Scholar
  67. Gerardy R, Zenk MH (1993) Formation of salutaridine from (R)-Reticuline by a membrane bound cytochrome P-450 enzyme from ‘Papaver somniferum’. Phytochemistry 32, Nr. 1:79–86Google Scholar
  68. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812PubMedGoogle Scholar
  69. Grandmaison J, Ibrahim RK (1996) Evidence for nuclear protein binding of flavonol sulfate esters in Flaveria chloraefolia. J Plant Physiol 147:653–660Google Scholar
  70. Grotewold E, Chamberlin M, Snook M, et al (1998) Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10:721–740PubMedGoogle Scholar
  71. Guo Z, Severson RF, Wagner GJ (1994) Biosynthesis of the diterpene cis-abienol in cell-free extracts of tobacco trichomes. Arch Biochem Biophys 308:103–108PubMedGoogle Scholar
  72. Guz NR, Stermitz FR, Johnson JB, et al (2001) Flavonolignan and flavone inhibitors of a Staphylococcus aureus multidrug resistance pump: structure – activity relationships. J Med Chem 44:261–268PubMedGoogle Scholar
  73. Haralampidis K, Bryan G, Qi X, et al (2001) A new class of oxidosqualene cyclases directs synthesis of antimicrobial phytoprotectants in monocots. Proc Natl Acad Sci USA 98:13431–13436PubMedGoogle Scholar
  74. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504PubMedGoogle Scholar
  75. Harborne JB, Williams CA, Greenham J, et al (1994) Variations in the lipophilic and vacuolar flavonoids of the genus Vellozia. Phytochemistry 35:1475–1480Google Scholar
  76. Harborne JB (1988) Flavonoids in the environment: structure-activity relationships. Prog Clin Biol Res 280:17–27PubMedGoogle Scholar
  77. Harper JF, Manney L, Sussman MR (1994) The plasma membrane H+ ATPase gene family in Arabidopsis: Genomic sequence of AHA10 which is expressed primarily in developing seeds. Mol Gen Genet 244:572–587PubMedGoogle Scholar
  78. Hartmann T. (1999) Chemical ecology of pyrrolizidine alkaloids. Planta, 207, 483–495Google Scholar
  79. Hashimoto T. Yamada Y. (1994) Alkaloid biogenesis: molecular aspects. Annu Rev Plant Physiol Plant Mol Biol, 45, 257–285.Google Scholar
  80. Hause B, Meyer K, Viitanen PV, et al (2002) Immunolocalization of 1-O-sinapoylglucose:malate sinapoyltransferase in Arabidopsis thaliana. Planta 215:26–32PubMedGoogle Scholar
  81. Hauser M-T, Wink M (1990) Uptake of alkaloids by latex vesicles and isolated mesophyll vacuoles of Chelidonium majus (Papaverceae). Z. Naturforsch 45c, 949–995Google Scholar
  82. Hinder B, Schellenberg M, Rodon S, et al (1996) How plants dispose of chlorophyll catabolites – Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem 271:27233–27236PubMedGoogle Scholar
  83. Hopp W, Seitz HU (1987) The uptake of acylated anthocyanin into isolated vacuoles from a cell suspension culture of Daucus carota. Planta 170:74–85Google Scholar
  84. Hsieh K, Huang AHC (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–596PubMedGoogle Scholar
  85. Hutzler P, Fischbach R, Heller W, et al (1998) Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J Exp Bot 49:953–965Google Scholar
  86. Ibrahim RK, De Luca V, Khouri H, et al (1987) Enzymology and compartmentation of polymethylated flavonol glucosides in Chrysosplenium americanum. Phytochemistry 26:1237–1245Google Scholar
  87. Ibrahim R (1990) Immunocytochemical localization of plant secondary metabolites and enzymes involved in their biosynthesis. Phytochem Anal 1:49–59Google Scholar
  88. Ikezawa N, Tanaka M, Nagayoshi M, et al (2003) Molecular cloning and characterization of CYP719, a methylenedioxy bridge-forming enzyme that belongs to a novel P450 family, from cultured Coptis japonica cells. J Biol Chem 278:38557–38565PubMedGoogle Scholar
  89. Irani NG, Grotewold E (2005) Light-induced morphological alteration in anthocyanin-accumulating vacuoles of maize cells. BMC Plant Biol 5:7PubMedGoogle Scholar
  90. Jans B (1974) Untersuchungen am Milchsaft des Schöllkrauts (Chelidonium majus) Ber. Schweiz Bot Ges 83:306–344Google Scholar
  91. Jasinski M, Stukkens Y, Degand H, et al (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107PubMedGoogle Scholar
  92. Jorgensen K, Rasmussen AV, Morant M, et al (2005) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr Opin Plant Biol 8:280–291PubMedGoogle Scholar
  93. Kaneda M, Rensing KH, Wong JCT, et al (2008) Tracking monolignols during wood development in lodgepole pine. Plant Physiol. 147:1750–1760PubMedGoogle Scholar
  94. Kempe I (2008) Analyse der Benzylisochinolinalkaloid-Biosynthese des Papaver somniferum L. mit Hilfe der RNAi-Technik. Dissertation (Ph.D.) Martin-Luther-Universität Halle, 2008.Google Scholar
  95. Kitamura S (2006) Transport of flavonoids. In: E Grotewold, ed, The science of flavonoids. Springer Science and Business Media, New York, pp 123–146Google Scholar
  96. Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114PubMedGoogle Scholar
  97. Klein M, Martinoia E, Hoffmann-Thoma G, et al (2000) A membrane-potential dependent ABC-like transporter mediates the vacuolar uptake of rye flavone glucuronides: regulation of glucuronide uptake by glutathione and its conjugates. Plant J 21:289–304PubMedGoogle Scholar
  98. Klein M, Martinoia E, Hoffmann-Thoma G, et al (2001) The ABC-like vacuolar transporter for rye mesophyll flavone glucuronides is not species-specific. Phytochemistry 56:153–159PubMedGoogle Scholar
  99. Klein M, Martinoia E, Weissenböck G (1997) Transport of lucifer yellow CH into plant vacuoles – evidence for direct energization of a sulphonated substance and implications for the design of new molecular probes. FEBS Lett 420:86–92PubMedGoogle Scholar
  100. Klein M, Martinoia E, Weissenböck G (1998) Directly energized uptake of ß-estradiol 17-(ß-D-glucuronide) in plant vacuoles is strongly stimulated by glutathione conjugates. J Biol Chem 273:262–270PubMedGoogle Scholar
  101. Klein M, Perfus-Barbeoch L, Frelet A, et al (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J 33:119–129PubMedGoogle Scholar
  102. Klein M, Weissenböck G, Dufaud A, et al (1996) Different energization mechanisms drive the vacuolar uptake of a flavonoid glucoside and a herbicide glucoside. J Biol Chem 271:29666–29671PubMedGoogle Scholar
  103. Kreuz K, Tommasini R, Martinoia E (1996) Old enzymes for a new job - Herbicide detoxification in plants. Plant Physiol 111:349–353PubMedGoogle Scholar
  104. Kutchan TM, Rush M, Coscia CJ (1986) Subcellular localization of alkaloids and dopamine in different vacuolar compartments of Papaver bracteatum. Plant Physiol 81:61–166Google Scholar
  105. Larsen ES, Alfenito MR, Briggs WR, et al (2003) A carnation anthocyanin mutant is complemented by the glutathione S-transferases encoded by maize Bz2 and petunia An9. Plant Cell Rep 21:900–904PubMedGoogle Scholar
  106. Latchinian-Sadek L, Ibrahim RK (1991) Flavonol ring B-specific O-glucosyltransferases: purification, production of polyclonal antibodies, and immunolocalization. Arch Biochem Biophys 289:230–236PubMedGoogle Scholar
  107. Lee KS, Tsien RW (1983) Mechanism of calcium channel blockade by verapamil, D600, diltiazem and nitrendipine in single dialysed heart cells. Nature 302:790–794PubMedGoogle Scholar
  108. Lehfeldt C, Shirley AM, Meyer K, et al (2000) Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 12:1295–1306PubMedGoogle Scholar
  109. Leier I, Jedlitschky G, Buchholz U, et al (1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J Biol Chem 269:27807–27810PubMedGoogle Scholar
  110. Lenz R, Zenk MH (1995) Purification and properties of codeinone reductase (NADPH) from Papaver somniferum cell cultures and differentiated plants. Eur J Biochem 233:132–139PubMedGoogle Scholar
  111. Lepiniec L, Debeaujon I, Routaboul JM, et al (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430PubMedGoogle Scholar
  112. Leslie EM, Deeley RG, Cole SPC (2003) Bioflavonoid stimulation of glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). Drug Metab Dispos 31:11–15PubMedGoogle Scholar
  113. Leslie EM, Mao Q, Oleschuk CJ, et al (2001) Modulation of multidrug resistance protein 1 (MRP1/ABCC1) transport and ATPase activities by interaction with dietary flavonoids. Mol Pharmacol 59:1171–1180PubMedGoogle Scholar
  114. Li ZS, Alfenito M, Rea PA, et al (1997) Vacuolar uptake of the phytoalexin medicarpin by the glutathione conjugate pump. Phytochemistry 45:689–693PubMedGoogle Scholar
  115. Li L, He Z, Pandey GK, et al (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277:5360–5368PubMedGoogle Scholar
  116. Li ZS, Szczypka M, Lu YP, et al (1996) The yeast cadmium factor protein (YCF1) is a vacuolar glutathione S-conjugate pump. J Biol Chem 271:6509–6517PubMedGoogle Scholar
  117. Li ZS, Zhao Y, Rea PA (1995) Magnesium ­adenosine 5’-triphosphate-energized transport of glutathione-S-conjugates by plant vacuolar membrane vesicles. Plant Physiol 107:1257–1268PubMedGoogle Scholar
  118. Lim EK, Li Y, Parr A, et al (2001) Identification of glucosyltransferase genes involved in sinapate metabolism and lignin synthesis in Arabidopsis. J Biol Chem 276: 4344–4349PubMedGoogle Scholar
  119. Lin Y, Irani NG, Grotewold E (2003) Sub-cellular trafficking of phytochemicals explored using auto-fluorescent compounds in maize cells. BMC Plant Biol 3:10PubMedGoogle Scholar
  120. Liu G, Sanchez-Fernandez R, Li ZS, et al (2001) Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J Biol Chem 276:8648–8656Google Scholar
  121. Loyola-Vargas VM, Broeckling CD, Badri D, et al (2007) Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta 225:301–310PubMedGoogle Scholar
  122. Lu YP, Li ZS, Rea PA (1997) AtMRP1 gene of Arabidopsis encodes a glutathione S-conjugate pump: isolation and functional definition of a plant ATP-binding cassette transporter gene. Proc Natl Acad Sci USA 94:8243–8248PubMedGoogle Scholar
  123. Lu YP, Li ZS, Drozdowicz YM, et al (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: Functional comparisons with AtMRP1. Plant Cell 10:267–282PubMedGoogle Scholar
  124. Luo B, Xue XY, Hu WL, et al (2007) An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol 48:1790–1802PubMedGoogle Scholar
  125. Madyastha KM, Ridgway JE, Dwyer JG, et al (1977) Subcellular localization of a cytochrome P-450-dependent monooxygenase in vesicles of the higher plant Catharanthus roseus. J Cell Biol 72:303–313Google Scholar
  126. Magalhaes JV, Liu J, Guimares CT, et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39:1156–1161PubMedGoogle Scholar
  127. Mahady GB, Beecher CW (1994) Quercetin-induced benzophenanthridine alkaloid production in suspension cell cultures of Sanguinaria canadensis. Planta Med 60:553–557PubMedGoogle Scholar
  128. Marinova K, Kleinschmidt K, Weissenböck G, et al (2007a) Flavonoid biosynthesis in barley primary leaves requires the presence of the vacuole and controls the activity of vacuolar flavonoid transport. Plant Physiol 144:432–444Google Scholar
  129. Marinova K, Pourcel L, Weder B, et al (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038PubMedGoogle Scholar
  130. Markham KR, Gould KS, Winefield CS, et al (2000) Anthocyanic vacuolar inclusions - their nature and significance in flower colouration. Phytochemistry 55:327–336PubMedGoogle Scholar
  131. Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158PubMedGoogle Scholar
  132. Marrs KA, Alfenito MR, Lloyd AM, et al (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375:397PubMedGoogle Scholar
  133. Martinoia E, Grill E, Tommasini R, et al (1993) ATP-dependent glutathione S-conjugate export pump in the vacuolar membrane of plants. Nature 364:247–249Google Scholar
  134. Martinoia E, Klein M, Sanchez-Fernandez R, et al (2000) Vacuolar uptake of secondary metabolites and xenobiotics. In: DG Robinson, JC Rogers, eds, Vacuolar compartments, Vol 5. Sheffield Academic Press, Sheffield, pp 221–253Google Scholar
  135. Masuda S, Terada T, Yonezawa A, et al (2006) Identification and functional characterization of a new human kidney-specific H+/organic cation antiporter, kidney-specific Multidrug and Toxin Extrusion 2. J Am Soc Nephrol 17:2127–2135PubMedGoogle Scholar
  136. Matern U (1987) Die Isomerenfall für Sekundärme-tabolite, eine Alternative zum Ionenfallen-Modell. Biologie in unserer Zeit 17:148–152Google Scholar
  137. Matern U, Heller W, Himmelspach K (1983) Conformational-changes of apigenin 7-O-(6-O-malonylglucoside), a vacuolar pigment from parsley, with solvent composition and proton concentration. Eur J Biochem 133:439–448PubMedGoogle Scholar
  138. Matern U, Reichenbach C, Heller W (1986) Efficient uptake of flavonoids into parsley (Petroselinum hortense) vacuoles requires acylated glycosides. Planta 167:183–189Google Scholar
  139. Matile P (1976) Lokalization of alkaloids and mechanism of their accumulation in vacuoles of Chelidonium majus lacticifers. Nova Acta Leopoldina, Suppl. Nr 7, Symposium Secondary Metabolism and Coevolution, 139–156Google Scholar
  140. Matile P (1984) Das toxische Kompartiment der Pflanzenzelle. Naturwiss. 71:18–24Google Scholar
  141. Matros A, Mock H-P (2004) Ectopic expression of a UDP-glucose:phenylpropanoid glucosyltransferase leads to increased resistance of transgenic tobacco plants against infection with Potato Virus Y. Plant Cell Physiol 45:1185–1193PubMedGoogle Scholar
  142. McKnight TD, Bergey DR, Burnett RJ, et al (1991) Expression of enzymatically active and correctly targeted strictosidine synthase in transgenic tobacco plants. Planta 185:148–152Google Scholar
  143. Morita Y, Kodama K, Shiota S, et al (1998) NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 42:1778–1782PubMedGoogle Scholar
  144. Morita Y, Kataoka A, Shiota S, et al (2000) NorM of Vibrio parahaemolyticus is an Na+-driven multidrug efflux pump. J Bacteriol 182:6694–6697PubMedGoogle Scholar
  145. Mueller LA, Goodman CD, Silady RA, et al (2000) AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. Plant Physiol 123:1561–1570PubMedGoogle Scholar
  146. Murata J, De Luca V (2005) Localization of tabersonine 16-hydroxylase and 16-OH tabersonine-16-O-methyltransferase to leaf epidermal cells defines them as a major site of precursor biosynthesis in the vindoline pathway in Catharanthus roseus. Plant J 44: 581–594PubMedGoogle Scholar
  147. Mylona P, Owatworakit A, Papadopoulou K, et al (2008) Sad3 and Sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20:201–212PubMedGoogle Scholar
  148. Nakagawa K, Konagai A, Fukui H, et al (1984) Release and crystallization of berberine in the liquid medium of Thalictrum minus cell suspension cultures. Plant Cell Reports 3:254–257Google Scholar
  149. Nawrath C, Heck S, Parinthawong N, et al (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286PubMedGoogle Scholar
  150. Nielsen KA, Gotfredsen CH, Buch-Pedersen MJ, et al (2004) Inclusions of flavonoid 3-deoxyanthocyanidins in Sorghum bicolor self-organize into spherical structures. Physiol Molec Plant Pathol 65:187–196Google Scholar
  151. Nozue M, Yasuda H (1985) Occurrence of anthocynoplasts in cell suspension culture of sweet potato. Plant Cell Reports 4:252–255Google Scholar
  152. Omote H, Hiasa M, Matsumoto T, et al (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27:587–593PubMedGoogle Scholar
  153. Ono E, Hatayama M, Isono Y, et al (2006) Localization of a flavonoid biosynthetic polyphenol oxidase in vacuoles. Plant J 45:133–143PubMedGoogle Scholar
  154. Onyilagha JC, Grotewold E (2004) The biology and structural distribution of surface flavonoids Recent Res Devel Plant Sci 2:1–18Google Scholar
  155. Osbourn AE (1996) Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8:1821–1831PubMedGoogle Scholar
  156. Osbourn AE (2003) Saponins in cereals. Phytochemistry 62:1–4PubMedGoogle Scholar
  157. Otani M, Shitan N, Sakai K, et al (2005) Characterization of vacuolar transport of the endogenous alkaloid berberine in Coptis japonica. Plant Physiol 138:1939–1946PubMedGoogle Scholar
  158. Otsuka M, Matsumoto T, Morimoto R, et al (2005) A human transporter protein that mediates the final excretion step for toxic organic cations. Proc Natl Acad Sci USA 102:17923–17928PubMedGoogle Scholar
  159. Panicot M, Minguet EG, Ferrando A, et al (2004) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14:2539–2551Google Scholar
  160. Panikashvili D, Savaldi-Goldstein S, Mandel T, et al (2007) The Arabidopsis DESPERADO/ AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345–1360PubMedGoogle Scholar
  161. Paulsen IT, Brown MH, Skurray RA (1996) Proton-dependent multidrug efflux systems. Microb Mol Biol Rev 60:575–608Google Scholar
  162. Pecket RC, Small CJ (1980) Occurrence, location and development of anthocyanoplasts. Phytochemistry 19:2571–2576Google Scholar
  163. Peer WA, Brown DE, Tague BW, et al (2001) Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis. Plant Physiol 126:536–548PubMedGoogle Scholar
  164. Peer WA, Bandyopadhyay A, Blakeslee JJ, et al (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911PubMedGoogle Scholar
  165. Pighin JA, Zheng H, Balakshin LJ, et al (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704PubMedGoogle Scholar
  166. Polster J, Dithmar H, Burgemeister R, et al W (2006) Flavonoids in plant nuclei: detection by laser microdissection and pressure catapulting (LMPC), in vivo staining, and UV-visible spectroscopic titration. Physiol Plant 128:163–174Google Scholar
  167. Poustka F, Irani NG, Feller A, et al (2007) A trafficking pathway for anthocyanins overlaps with the endoplasmic reticulum-to-vacuole protein-sorting route in Arabidopsis and contributes to the formation of vacuolar inclusions. Plant Physiol 145:1323–1335PubMedGoogle Scholar
  168. Rasmussen S, Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11:1537–1552PubMedGoogle Scholar
  169. Rataboul P, Alibert G, Boller T, et al (1985) Intracellular transport and vacuolar accumulation of o-coumaric acid glucoside in Melilotus alba mesophyll cell protoplasts. Biochim Biophys Acta 816:25–36Google Scholar
  170. Rea PA, Li ZS, Lu YP, et al (1998) From vacuolar GS-X pumps to multispecific ABC transporters. Annu Rev Plant Physiol Plant Mol Biol 49:727–760PubMedGoogle Scholar
  171. Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799PubMedGoogle Scholar
  172. Roos, W., Luckner, M. (1986) The spatial organization of secondary metabolism in microbial and plant cells. In: T. A. V. Subramanian, ed, Cell metabolism: growth and environment, Vol. 1. CRC Press, Boca Raton, FL, pp 45–73Google Scholar
  173. Rueffer M, Amman M, Zenk MH (1986) S-Adenosyl-L-methionine: columbamine-O-methyl transferase, a compartmentalized enzyme in protoberberine biosynthesis. Plant Cell Rep 3:182–185Google Scholar
  174. Russel FGM, Koenderink JB, Masereeuw R (2008) Multidrug resistance protein 4 (MRP4/ABCC4): a versatile efflux transporter for drugs and signalling molecules. Trends Pharmacol Sci 29: 200–207PubMedGoogle Scholar
  175. Saier MH, Jr., Paulsen IT (2001) Phylogeny of multidrug transporters. Semin Cell Dev Biol 12:205–213PubMedGoogle Scholar
  176. Saito K, Suzuki H, Takamatsu S, Murakoshi I, (1992) Acyltransferases for lupin alkaloids in Lupinus hirsutus. Phytochemistry 32: 87–91Google Scholar
  177. Sakai K, Shitan N, Sato F, et al (2002) Characterization of berberine transport into Coptis japonica cells and the involvement of ABC protein. J Exp Bot 53:1879–1886PubMedGoogle Scholar
  178. Samanani N, Alcantara J, Bourgault R, et al (2006) The role of phloem sieve elements and laticifers in the biosynthesis and accumulation of alkaloids in opium poppy. Plant J 47:547–563PubMedGoogle Scholar
  179. Samanani N, Park SU, Facchini PJ (2005) Cell type-specific localization of transcripts encoding nine consecutive enzymes involved in protoberberine alkaloid biosynthesis. Plant Cell 17:915–926PubMedGoogle Scholar
  180. Santelia D, Henrichs S, Vincenzetti V, et al (2008). Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J. Biol. Chem. 283:31218–31226.PubMedGoogle Scholar
  181. Saslowsky DE, Warek U, Winkel BS (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Biol Chem 280:23735–23740PubMedGoogle Scholar
  182. Schmeller T, Latz-Brüning B, Wink M (1997) Biochemical activities of berberine, palmatine and sanguinarine mediating chemical defence against microorganisms and herbivores. Phytochemistry 44:257–266PubMedGoogle Scholar
  183. Schulz B, Frommer WB (2004) A plant ABC transporter takes the lotus seat. Science 306:622–625PubMedGoogle Scholar
  184. Schulz M, Weissenböck G (1986) Isolation and separation of epidermal and mesophyll protoplasts from rye primary leaves – tissue specific characteristics of secondary phenolic product accumulation. Z Naturforsch [C] 41:22–27Google Scholar
  185. Schumacher HM, Zenk MH (1988) Partial purification and characterization of dihydrobenzophenanthridine oxidase from Eschscholtzia californica cell suspension cultures. Plant Cell Rep 7:43–46Google Scholar
  186. Sharma V, Strack D (1985) Vacuolar localization of 1-sinapolglucose: l-malate sinapoyltransferase in protoplasts from cotyledons of Raphanus sativus. Planta 163:563–568Google Scholar
  187. Shiono M, Matsugaki N, Takeda K (2005) Phytochemistry: structure of the blue cornflower pigment. Nature 436:791PubMedGoogle Scholar
  188. Shirley AM, McMichael CM, Chapple C (2001) The sng2 mutant of Arabidopsis is defective in the gene encoding the serine carboxypeptidase-like protein sinapoylglucose:choline sinapoyltransferase. Plant J 28:83–94PubMedGoogle Scholar
  189. Shirley AM, Chapple C (2003) Biochemical characterization of sinapoylglucose:choline sinapoyltransferase, a serine carboxypeptidase-like protein that functions as an acyltransferase in plant secondary metabolism. J Biol Chem 278:19870–19877PubMedGoogle Scholar
  190. Shitan N, Bazin I, Dan K, et al (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
  191. Shitan N, Kiuchi F, Sato F, Yazaki K, Yoshimatsu K. (2005) Establishment of Rhizobium-mediated transformation of Coptis japonica and molecular analyses of transgenic plants. Plant Biotechnol., 22,:113–118.Google Scholar
  192. Shitan N, Yazaki K (2007) Accumulation and membrane transport of plant alkaloids. Current Pharmaceutical Biotechnology 8:244–252PubMedGoogle Scholar
  193. Slaninova I., Taborska E, Bochorakova H, et al (2001) Interaction of benzo[c]phenanthridine and protoberberine alkaloids with animal and yeast cells. Cell Biol Toxicol 17:51–63PubMedGoogle Scholar
  194. Small CJ, Pecket RC (1982) The ultrastructure of anthocyanoplasts in red cabbage. Planta 154:97–99Google Scholar
  195. Snyder BA, Nicholson RL (1990) Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248:1637–1639PubMedGoogle Scholar
  196. Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482PubMedGoogle Scholar
  197. Spelt C, Quattrocchio F, Mol J, et al (2002) ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms. Plant Cell 14:2121–2135PubMedGoogle Scholar
  198. St-Pierre B, Vazquez-Flota FA, De Luca V (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:887–900PubMedGoogle Scholar
  199. St-Pierre B, De Luca V (1995) A cytochrome P-450 monooxygenase catalyzes the first step in the conversion of tabersonine to vindoline in Catharanthus roseus. Plant Physiol 109:131–139PubMedGoogle Scholar
  200. Stafford HA (1990) Flavonoid metabolism. CRC Press, Boca Raton, FLGoogle Scholar
  201. Stermitz FR, Lorenz P, Tawara JN, et al (2000) Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 5’-methoxyhydnocarpin, a multidrug pump inhibitor. PROC NATL ACAD SCI USA 97:1433–1437PubMedGoogle Scholar
  202. Stevens LH, Blom TJM, Verpoorte R (1993) Subcellular localization of tryptophan decarboxylase, strictosidine synthase and strictosidine glucosidase in suspension cultured cells of Catharanthus roseus and Tabernaemontana divaricata. Plant Cell Rep 12:563–576Google Scholar
  203. Strack D (1982) Development of 1-O-sinapoyl-b-D-glucose: L-malate sinapoyltransferase activity in cotyledons of red radish (Raphanus sativus L. var. sativus). Planta 155:31–36Google Scholar
  204. Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-rhizobium symbiosis. Plant Physiol 144:2000–2008PubMedGoogle Scholar
  205. Suzuki H, Koike Y, Murakoshi I, et al (1996) Subcellular localization of acyltransferases for quinolizidine alkaloid biosynthesis in Lupinus. Phytochemistry 42:1557–1562Google Scholar
  206. Taguchi G, Fujikawa S, Yazawa T, et al (2000) Scopoletin uptake from culture medium and accumulation in the vacuoles after conversion to scopolin in 2,4-D-treated tobacco cells. Plant Sci 151:153–161PubMedGoogle Scholar
  207. Terasaka K, Sakai K, Sato F, et al (2003) Thalictrum minus cell cultures and ABC-like transporter. Phytochemistry 62:483–489PubMedGoogle Scholar
  208. Ukitsu H, Kuromori T, Toyooka K, et al (2007) Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant Cell Physiol 48:1524–1533PubMedGoogle Scholar
  209. Valant-Vetschera KM, Wollenweber E (2001) Exudate flavonoid aglycones in the alpine species of Achillea sect. Ptarmica: Chemosystematics of A. moschata and related species (Compositae-Anthemideae). Biochem Syst Ecol 29:149–159PubMedGoogle Scholar
  210. Valant-Vetschera KM, Wollenweber E, Faure R, et al (2003) New exudate flavonoids of species from the Chrysanthemum complex (Asteraceae-Anthemideae). Biochem Syst Ecol 31:545–548Google Scholar
  211. Verrier PJ, Bird D, Burla B, et al (2008) Plant ABC proteins – a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159PubMedGoogle Scholar
  212. Viehweger K, Lein W, Schumann B, Roos W, et al (2006). A G protein controls a pH dependent signal path to the induction of phytoalexin biosynthesis in Eschscholzia californica. Plant Cell 18:1510–1523PubMedGoogle Scholar
  213. Walczak HA, Dean JV (2000) Vacuolar transport of the glutathione conjugate of trans-cinnamic acid. Phytochemistry 53:441–446PubMedGoogle Scholar
  214. Walker TS, Bais HP, Grotewold E, et al (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedGoogle Scholar
  215. Wang E, Wagner GJ (2003) Elucidation of the functions of genes central to diterpene metabolism in tobacco trichomes using posttranscriptional gene silencing. Planta 216:686–691PubMedGoogle Scholar
  216. Wang J, Raman H, Zhou M, et al (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115:265–276PubMedGoogle Scholar
  217. Weid M, Ziegler J, Kutchan TM (2004) The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci USA 101:13957–13962PubMedGoogle Scholar
  218. Weiss D, Baumert A, Vogel M, Roos W (2006) Sanguinarine reductase, a key enzyme of benzophenanthridine detoxification. Plant Cell Environ 29:291–302PubMedGoogle Scholar
  219. Weisskopf L, Abou-Mansour E, Fromin N, et al (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29:919–927PubMedGoogle Scholar
  220. Werner C, Matile P (1985) Accumulation of coumarylglucosides in vacuoles of barley mesophyll protoplasts. J Plant Physiol 118:237–249Google Scholar
  221. Wink M (1997) Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. In: RA Leigh, D Sanders, JA Callow, eds, The plant vacuole. Advances in Botanical Reserach, Vol 25. Academic Press, London/New York, pp 141–169Google Scholar
  222. Wink M, Roberts MF (1998) Compartmentation of alkaloid biosynthesis, transport and storage. In: Roberts MF, Wink M eds, Alkaloids: biochemistry, ecology and medicinal applications, Plenum Press, New York, pp 239–262Google Scholar
  223. Wink M, Schmeller T, Latz-Bruning B (1998) Modes of action of allelochemical alkaloids: Interaction with neuroreceptors, DNA, and other molecular targets. J Chem Ecol 24:1881–1937Google Scholar
  224. Winkel BS (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107PubMedGoogle Scholar
  225. Wolff J, Knipling L (1993) Antimicrotubule properties of benzophenanthridine alkaloids. Biochem 32:13334–13339Google Scholar
  226. Wollenweber E, Dorr M, Rivera D, et al (2003) Externally accumulated flavonoids in three Mediterranean Ononis species. Z Naturforsch [C] 58:771–775Google Scholar
  227. Wu CP, Calcagno AM, Hladky SB, Ambudkar SV, Barrand MA (2005) Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J. 272: 4725–4740PubMedGoogle Scholar
  228. Xu LF, Chu WJ, Qing XY, et al (2006) Protopine inhibits serotonin transporter and noradrenaline transporter and has the antidepressant-like effect in mice models. Neuropharmacology 50:934–940PubMedGoogle Scholar
  229. Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307PubMedGoogle Scholar
  230. Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580:1183–1191PubMedGoogle Scholar
  231. Yazaki K, Shitan N, Takamatsu H, et al (2001) A novel Coptis japonica multidrug resistance protein preferentially expressed in the alkaloid-accumulating rhizome. J Exp Bot 52: 877–879PubMedGoogle Scholar
  232. Yazaki K, Sugiyama A, Morita M, et al (2007) Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phytochem Rev. DOI 10.1007/s11101-007-9079-8Google Scholar
  233. Zenk MH (1994) The formation of benzophenanthridine alkaloids. Pure Appl Chem 66:2023–2028Google Scholar
  234. Zhang H, Wang L, Deroles S, et al (2006) New insight into the structures and formation of anthocyanic vacuolar inclusions in flower petals. BMC Plant Biology 6:29PubMedGoogle Scholar
  235. Ziegler J, Facchini PJ (2008) Alkaloid Biosynthesis: Metabolism and Trafficking. Annu Rev Plant Biol 59:735–769PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Zurich Basel Plant Science CenterUniversity of Zurich, Plant BiologyZurichSwitzerland
  2. 2.Pharmaceutical Biology, Molecular Cell BiologyMartin-Luther University Halle-WittenbergHalleGermany
  3. 3.Philip Morris Products S.A. ,NeuchâtelSwitzerland

Personalised recommendations