Molecular cloning and functional characterization of Catharanthus roseus hydroxymethylbutenyl 4-diphosphate synthase gene promoter from the methyl erythritol phosphate pathway

详细信息    查看全文

• 作者：Olivia Ginis (1)
  Vincent Courdavault (1)
  Céline Melin (1)
  Arnaud Lanoue (1)
  Nathalie Giglioli-Guivarc’h (1)
  Benoit St-Pierre (1)
  Martine Courtois (1)
  Audrey Oudin (1) audrey.oudin@univ-tours.fr
• 关键词：Promoter – Hydroxymethylbutenyl 4 ; diphosphate synthase gene – Methyl erythritol phosphate pathway – Monoterpenoid indole alkaloids – Catharanthus roseus – GUS activity
• 刊名：Molecular Biology Reports
• 出版年：2012
• 出版时间：May 2012
• 年：2012
• 卷：39
• 期：5
• 页码：5433-5447
• 全文大小：642.3 KB
• 参考文献：1. Guirimand G, Courdavault V, Lanoue A, Mahroug S, Guihur A, Blanc N, Giglioli-Guivarc’h N, St-Pierre B, Burlat V (2010) Strictosidine activation in Apocynaceae: towards a “nuclear time bomb”? BMC Plant Biol 10:182. doi:
  2. Roepke J, Salim V, Wu M, Thamm AMK, Murata J, Ploss K, Boland W, De Luca V (2010) Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle. Proc Natl Acad Sci USA 107:15287–15292. doi:
  3. van der Heijden R, Jacobs D, Snoeijer W, Hallard D, Verpoorte R (2004) The catharanthus alkaloids: pharmacognosy and biotechnology. Curr Med Chem 11:607–628
  4. Ziegler J, Facchini PJ (2008) Alkaloid biosynthesis: metabolism and trafficking. Annu Rev Plant Biol 59:735–769. doi:
  5. Guirimand G, Courdavault V, St-Pierre B, Burlat V (2010) Biosynthesis and regulation of alkaloids. In: Pua EC, Davey M (eds) Plant developmental biology—biotechnological perspectives, vol 2. Springer, Berlin, pp 139–160
  6. Oudin A, Courtois M, Rideau M, Clastre M (2007) The iridoidpathway in Catharanthus roseus alkaloid biosynthesis. Phytochem Rev 6:259–276. doi:
  7. Chahed K, Oudin A, Giglioli-Guivarc’h N, Hamdi S, Chénieux JC, Rideau M, Clastre M (2000) 1-Deoxy-d-xylulose 5-phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid-producing cells. Plant Physiol Biochem 38:559–566. doi:
  8. Veau B, Courtois M, Oudin A, Chénieux JC, Rideau M, Clastre M (2000) Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochim Biophys Acta 1517:159–163. doi:
  9. Oudin A, Mahroug S, Courdavault V, Hervouet N, Zelwer C, Rodriguez-Concepcion M, St-Pierre B, Burlat V (2007) Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. Plant Mol Biol 65:13–30. doi:
  10. Giglioli-Guivarc’h N, Courdavault V, Oudin A, Crèche J, St-Pierre B (2006) Madagascar periwinkle, an attractive model for studying the control of the biosynthesis of terpenoid derivative compounds. In: Teixeira Da Silva JA (ed) Floriculture, ornamental and plant biology, vol 2. Global Science Books, Isleworth
  11. Mérillon JM, Ouelhazi L, Doireau P, Chénieux JC, Rideau M (1989) Metabolic changes and alkaloid production in habituated and non-habituated cells of Catharanthus roseus grown in hormone free-medium. Comparing hormone-deprived non-habituated cells with habituated cells. J Plant Physiol 134:54–60
  12. Arvy MP, Imbault N, Naudascher F, Thiersault M, Doireau P (1994) 2, 4-D and alkaloid accumulation in periwinkle cell suspensions. Biochimie 76(5):410–416
  13. Décendit A, Liu D, Ouelhazi L, Doireau P, Mérillon JM, Rideau M (1992) Cytokinin-enhanced accumulation of indole alkaloids in Cathranthus roseus cell-cultures: the factors affecting the cytokinin response. Plant Cell Rep 11(8):400–403. doi:
  14. Décendit A, Petit G, Andreu F, Doireau P, Mérillon JM, Rideau M (1993) Putative sites of cytokinin action during their enhancing effect on indole alkaloid accumulation periwinkle cell suspensions. Plant Cell Rep 12(12):710–712. doi:
  15. Yahia A, Kevers C, Gaspar T, Chénieux JC, Rideau M, Crèche J (1998) Cytokinins and ethylene stimulate indole alkaloids accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms. Plant Sci 133:9–15. doi:
  16. Guirimand G, Guihur A, Ginis O, Poutrain P, Héricourt F, Oudin A, Lanoue A, St-Pierre B, Burlat V, Courdavault V (2011) The subcellular organisation of the strictosidine biosynthesis in Catharanthus roseus epidermis highlights several trans-tonoplast translocations of intermediate metabolites. FEBS J 278(5):749–763. doi:
  17. Courdavault V, Burlat V, St-Pierre B, Giglioli-Guivarc’h N (2005) Characterisation of CaaX-prenyltransferases in Catharanthus roseus: relationships with the expression of genes involved in the early stages of monoterpenoid biosynthetic pathway. Plant Sci 168:1097–1107. doi:
  18. Broun P (2004) Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7(2):202–209. doi:
  19. Memelink J, Verpoorte R, Kijne JW (2001) ORCAnisation of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219. doi:
  20. Memelink J (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry 70(13–14):1560–1570. doi:
  21. van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297. doi:
  22. van der Fits L, Memelink J (2001) The jasmonate-inducible AP2/ERF domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. Plant J 25:43–53. doi:
  23. Siberil Y, Benhamron S, Memelink J, Giglioli-Guivarc’h N, Thiersault M, Boisson B, Doireau P, Gantet P (2001) Catharanthus roseus G-box binding factors 1 and 2 act as repressors of strictosidine synthase gene expression in cell cultures. Plant Mol Biol 45:477–488. doi:
  24. Pauw B, Hilliou FAO, Martin VS, Chatel G, de Wolf CJF, Champion A, Pre M, van Duijn B, Kijne JW, van der Fits L, Memelink J (2004) Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus. J Biol Chem 279(51):52940–52948. doi:
  25. Menke FLH, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18(16):4455–4463. doi:
  26. Suttipanta N, Pattanaik S, Gunjan S, Xie CH, Littleton J, Yuan L (2007) Promoter analysis of the Catharanthus roseus geraniol 10-hydroxylase gene involved in terpenoid indole alkaloid biosynthesis. Biochim Biophys Acta 1769(2):139–148. doi:
  27. Liu YG, Huang N (1998) Efficient amplification of insert end sequences from bacterial artificial chromosome clones by thermal asymmetric interlaced PCR. Plant Mol Biol Rep 16:175–181. doi:
  28. Li ZT, Gray DJ (2005) Isolation by improved thermal asymmetric interlaced PCR and characterization of a seed specific 2S albumin gene and its promoter from grape (Vitis vinifera L.). Genome 48:312–320. doi:
  29. Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. Cabios 7:203–206
  30. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300
  31. Rombauts S, Dhais P, Van Montagu M, Rouz P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27(1):295–296. doi:
  32. Lescot M, Déhais P, Moreau Y, De Moor B, Rouzé P, Rombauts S (2002) PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. doi:
  33. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158
  34. Guirimand G, Burlat V, Oudin A, Lanoue A, St-Pierre B, Courdavault V (2009) Optimization of the transient transformation of Catharanthus roseus cells by particle bombardment and its application to the subcellular localization of hydroxymethylbutenyl 4-diphosphate synthase and geraniol 10-hydroxylase. Plant Cell Rep 28:1215–1234. doi:
  35. Courdavault V, Thiersault M, Courtois M, Gantet P, Oudin A, Doireau P, St-Pierre B, Giglioli-Guivarc’h N (2005) CaaXprenyltransferases are essential for expression of genes involved in the early stages of monoterpenoid biosynthetic pathway in Catharanthus roseus cells. Plant Mol Biol 57:855–870. doi:
  36. Jefferson RA, Kavanagh TA, Bevan MW (1987) Gus fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907
  37. 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 11:887–900. doi:
  38. Sakai H, Aoyama T, Oka A (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J 24:703–711. doi:
  39. Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16(5):1077–1090. doi:
  40. Fusada N, Masuda T, Kuroda H, Shimada H, Ohta H, Takamiya K (2005) Identification of a novel cis-element exhibiting cytokinin-dependent protein binding in vitro in the 5′-region of NADPH-protochlorophyllide oxidoreductase gene in cucumber. Plant Mol Biol 59(4):631–645. doi:
  41. Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17(2):209–214. doi:
  42. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57(2):155–171. doi:
  43. Montgomery J, Goldman S, Deikman J, Margossian L, Fischer RL (1993) Identification of an ethylene-responsive region in the promoter of a fruit ripening gene. Proc Natl Acad Sci USA 90(13):5939–5943
  44. Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50(1):43–57. doi:
  45. Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4(6):210–216. doi:
  46. Terzaghi WB, Cashmore AR (1995) Photomorphogenesis. Seeing the light in plant development. Curr Biol 5(5):466–468. doi:
  47. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5(11):1529–1539. doi:
  48. Cercós M, Gómez-Cadenas A, Ho TH (1999) Hormonal regulation of a cysteine proteinase gene, EPB-1, in barley aleurone layers: cis- and trans-acting elements involved in the co-ordinated gene expression regulated by gibberellins and abscisic acid. Plant J 19(2):107–118. doi:
  49. Plesch G, Ehrhardt T, Mueller-Roeber B (2001) Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J 28(4):455–464. doi:
  50. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206. doi:
  51. Baumann K, De Paolisa A, Costantino P, Gualberti G (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11:323–334. doi:
  52. Nakano T, Suzuki K, Ohtsuki N, Tsujimoto Y, Fujimura T, Shinshi H (2006) Identification of genes of the plant-specific transcription-factor families cooperatively regulated by ethylene and jasmonate in Arabidopsis thaliana. J Plant Res 119(4):407–413. doi:
  53. Yoo SY, Bomblies K, Yoo SK, Yang JW, Choi MS, Lee JS, Weigel D, Ahn JH (2005) The 35S promoter used in a selectable marker gene of a plant transformation vector affects the expression of the transgene. Planta 221(4):523–530. doi:
  54. Zheng XL, Deng W, Luo KM, Duan H, Chen YQ, McAvoy R, Song SQ, Pei Y, Li Y (2007) The cauliflower mosaic virus (CaMV) 35S promoter sequence alters the level and patterns of activity of adjacent tissue- and organ-specific gene promoters. Plant Cell Rep 26(8):1195–1203. doi:
  55. Gantet P, Imbault N, Thiersault M, Doireau P (1998) Necessity of a functional octadecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium. Plant Cell Phys 39(2):220–225
  56. Rose AB (2008) Intron-mediated regulation of gene expression. Curr Top Microbiol Immunol 326:277–290
  57. van der Fits L, Memelink J (1997) Comparison of the activities of CaMV 35S and FMV 34S promoter derivatives in Catharanthus roseus cells transiently and stably transformed by particle bombardment. Plant Mol Biol 33(5):943–946. doi:
  58. Hilliou F, Christou P, Leech MJ (1999) Development of an efficient transformation system for Catharanthus roseus cell cultures using particle bombardment. Plant Sci 140(2):179–188
  59. Montiel G, Breton C, Thiersault M, Burlat V, Jay-Allemand C, Gantet P (2007) Transcription factor Agamous-like 12 from Arabidopsis promotes tissue-like organization and alkaloid biosynthesis in Catharanthus roseus suspension cells. Metabol Eng 9(2):125–132. doi:
  60. Burlat V, Oudin A, Courtois M, Rideau M, St-Pierre B (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 38:131–141. doi:
  61. Estevez JM, Cantero A, Romero C, Kawaide H, Jimenez LF, Kuzuyama T, Seto H, Kamiya Y, Leon P (2000) Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-d-erythritol-4-phosphate pathway in Arabidopsis. Plant Phys 124:95–103. doi:
  62. Carretero-Paulet L, Ahumada I, Cunillera N, Rodriguez-Concepcion M, Ferrer A, Boronat A, Campos N (2002) Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-d-xylulose 5-phosphate reductoisomerase, the firstcommitted enzyme of the 2-C-methyl-d-erythritol 4-phosphate pathway. Plant Physiol 129:1581–1591. doi:
  63. Papon N, Bremer J, Vansiri A, Andreu F, Rideau M, Crèche J (2005) Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells. Planta Med 71:572–574. doi:
  64. Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45(4):386–391. doi:
  65. Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-cadinene synthase-A. Plant Phys 135:507–515. doi:
  66. Kato N, Dubouzet E, Kokabu Y, Yoshida S, Taniguchi Y, Dubouzet JG, Sato F, Yazaki K (2007) Identification of a WRKY protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in Coptis japonica. Plant Cell Phys 48(1):8. doi:
  67. Ma DM, Pu GB, Lei CY, Ma LQ, Wang HH, Guo YW, Chen JL, Du ZG, Wang H, Li GF, Ye HC, Liu BY (2009) Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the Amorpha-4, 11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Phys 50(12):2146. doi:
• 作者单位：1. Université Fran?ois Rabelais de Tours, EA 2106, Biomolécules et Biotechnologies Végétales, 31 avenue Monge, 37200 Tours, France
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Animal Anatomy, Morphology and Histology
  Animal Biochemistry
  
• 出版者：Springer Netherlands
• ISSN：1573-4978

文摘

The Madagascar periwinkle produces monoterpenoid indole alkaloids (MIA) of high interest due to their therapeutical values. The terpenoid moiety of MIA is derived from the methyl erythritol phosphate (MEP) and seco-iridoid pathways. These pathways are regarded as the limiting branch for MIA biosynthesis in C. roseus cell and tissue cultures. In previous studies, we demonstrated a coordinated regulation at the transcriptional and spatial levels of genes from both pathways. We report here on the isolation of the 5′-flanking region (1,049 bp) of the hydroxymethylbutenyl 4-diphosphate synthase (HDS) gene from the MEP pathway. To investigate promoter transcriptional activities, the HDS promoter was fused to GUS reporter gene. Agrobacterium-mediated transformation of young tobacco leaves revealed that the cloned HDS promoter displays a tissue-specific GUS staining restricted to the vascular region of the leaves and limited to a part of the vein that encompasses the phloem in agreement with the previous localization of HDS transcripts in C. roseus aerial organs. Further functional characterizations in stably or transiently transformed C. roseus cells allowed us to identify the region that can be consider as the minimal promoter and to demonstrate the induction of HDS promoter by several hormonal signals (auxin, cytokinin, methyljasmonate and ethylene) leading to MIA production. These results, and the bioinformatic analysis of the HDS 5′-region, suggest that the HDS promoter harbours a number of cis-elements binding specific transcription factors that would regulate the flux of terpenoid precursors involved in MIA biosynthesis.