Proteins prenylated by type I protein geranylgeranyltransferase act positively on the jasmonate signalling pathway triggering the biosynthesis of monoterpene indole alkaloids in Catharanthus roseus

Plant Cell Reports

Volumn 28, Issue 1, 2009, Pages 83-93

  Courdavault, Vincent ^a   Burlat, Vincent ^a   St Pierre, Benoit ^a   Giglioli Guivarc'h, Nathalie ^a  

^a UNIVERSITÉ DE TOURS   (France)

Author keywords

Alkaloid; Catharanthus roseus; Jasmonate; Protein prenylation; Type I protein geranylgeranyltransferase

Indexed keywords

ACETIC ACID DERIVATIVE; AJMALICINE; CYCLOPENTANE DERIVATIVE; GERANYLGERANYLTRANSFERASE TYPE I; GERANYLGERANYLTRANSFERASE TYPE-I; JASMONIC ACID METHYL ESTER; ORCA3 PROTEIN, PLANT; OXYLIPIN; PLANT RNA; RAUWOLFIA ALKALOID; TRANSCRIPTION FACTOR; TRANSFERASE; VEGETABLE PROTEIN;

ARTICLE; CATHARANTHUS; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN PRENYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ACETIC ACIDS; ALKYL AND ARYL TRANSFERASES; CATHARANTHUS; CELLS, CULTURED; CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; OXYLIPINS; PLANT PROTEINS; PROTEIN PRENYLATION; RNA INTERFERENCE; RNA, PLANT; SECOLOGANIN TRYPTAMINE ALKALOIDS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

CATHARANTHUS ROSEUS;

EID: 58149251985     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-008-0610-1     Document Type: Article

References (65)

1. MJ Adjobo-Hermans J Goedhart TWJ Gadella Jr 2006 Plant G protein heterotrimers require dual lipidation motifs of Galpha and Ggamma and do not dissociate upon activation J Cell Sci 119 5087 5097 10.1242/jcs.03284
2. R Aerts D Gisi E De Carolis V De Luca TW Baumann 1994 Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings Plant J 5 635 643
3. GJ Allen Y Murata SP Chu M Nafisi JI Schoeder 2002 Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2 Plant Cell 14 1649 1662 10.1105/tpc.010448
4. M-P Arvy N Imbault F Naudascher M Thiersault P Doireau 1994 2, 4-D and alkaloid accumulation in periwinkle cell suspensions Biochimie 76 410 416
5. O Barth W Zschiesche S Siersleben K Humbeck 2004 Isolation of a novel cDNA encoding a nuclear protein involved in stress response and leaf senescence Physiol Plant 121 282 293 10.1111/j.0031-9317.2004.00325.x
6. SM Brady SF Sarkar D Bonetta P McCourt 2003 The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis Plant J 34 67 75 10.1046/j.1365-313X.2003.01707.x
7. D Caldelari H Sternberg M Rodriguez-Concepcion W Gruissem S Yalovsky 2001 Efficient prenylation by a plant geranylgeranyltransferase-I requires a functional CaaL box motif and a proximal polybasic domain Plant Physiol 126 1416 1429
8. K Chahed A Oudin N Guivarc'h S Hamdi JC Chénieux M Rideau M Clastre 2000 I-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
9. D Chakravorty JR Botella 2007 Over-expression of a truncated Arabidopsis thaliana heterotrimeric G protein gamma subunit results in a phenotype similar to α and β subunit knockouts Gene 393 163 170 10.1016/j.gene.2007.02. 008
10. A Chini S Fonseca G Fernandez B Adie JM Chico O Lorenzo G Garcia-Casado I Lopez-Vidriero FM Lozano MR Ponce JL Micol R Solano 2007 The JAZ family of repressors is the missing link in jasmonate signalling Nature 448 666 671 10.1038/nature06006
11. G Collu N Unver AM Peltenburg-Looman R van der Heijden R Verpoort J Memelink 2001 Geraniol 10-hydroxylase, a cytochrome P450 enzyme involved in terpenoid indole alkaloid biosynthesis FEBS Lett 508 215 220 10.1016/S0014-5793(01)03045-9
12. A Contin R van der Heijden AW Lefebre R Verpoorte 1998 The iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture FEBS Lett 4 413 416
13. V Courdavault V Burlat P Gantet B St-Pierre N Giglioli-Guivarc'h 2005 Isolation of a cDNA encoding the alpha subunit of CaaX-prenyltransferase from Catharanthus roseus and expression of an active recombinant protein farnesyltransferase Cell Mol Biol Lett 10 649 657
14. Courdavault V, Burlat V, St-Pierre B, Giglioli-Guivarc'h (2005b) 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: 10.1016/j.plantsci.2004.12.010
15. V Courdavault M Thiersault M Courtois P Gantet A Oudin P Doireau B St-Pierre N Giglioli-Guivarc'h 2005 CaaX-prenyltransferases 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 10.1007/s11103-005-3095-0
16. S Cutler M Ghassemian D Bonetta S Cooney P McCourt 1996 A protein farnesyltransferase involved in abscisic acid signal transduction in Arabidopsis Science 273 1239 1241
17. V De Luca C Marineau N Brisson 1989 Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases Proc Natl Acad Sci USA 86 2582 2586
18. A de Waal AH Meijer R Verpoorte 1995 Strictosidine synthase from Catharanthus roseus : purification and characterization of multiple forms Biochem J 306 571 580
19. A Décendit D Liu L Ouelhazi P Doireau JM Mérillon M Rideau 1992 Cytokinin-enhanced accumulation of indole alkaloids in Catharanthus roseus cell cultures. The factors affecting the cytokinin response Plant Cell Rep 11 400 403
20. M El-Sayed R Verpoorte 2005 Methyljasmonate accelerates catabolism of monoterpenoid indole alkaloids in Catharanthus roseus during leaf processing Fitoterapia 76 83 90 10.1016/j.fitote.2004.10.019
21. A Galichet W Gruissem 2003 Protein farnesylation in plants-conserved mechanisms but different targets Curr Opin Plant Biol 6 530 535 10.1016/j.pbi.2003.09.005
22. A Galichet W Gruissem 2006 Developmentally controlled farnesylation modulates AtNAP1;1 function in cell proliferation and cell expansion during Arabidopsis leaf development Plant Physiol 142 1412 1426
23. A Galichet K Hoyerova M Kaminek W Gruissem 2008 Farnesylation directs AtIPT3 subcellular localization and modulates cytokinin biosynthesis in Arabidopsis Plant Physiol 146 1155 1164 /10.1104/pp.107.107425
24. OL Gamborg RRA Miller K Ojima 1968 Nutriment requirements of suspension cultures of soybean root cells Exp Cell Res 50 151 158
25. P Gantet N Imbault M Thiersault P Doireau 1997 Inhibition of alkaloid accumulation by 2, 4-D in Catharanthus roseus cell suspension is overcome by methyljasmonate Acta Bot Gallica 122 783 786
26. P Gantet N Imbault M Thiersault P Doireau 1998 Necessity of a functional octadecanoic pathway for indole alkaloid synthesis by Catharanthus roseus cell suspensions cultured in an auxin-starved medium Plant Cell Physiol 39 220 225
27. MH Gelb F Tamanoi K Yokoyama F Ghomashchi K Esson MN Gould 1995 The inhibition of protein prenyltransferases by oxygenated metabolites of limonene and perillyl alcohol Cancer Lett 91 169 175
28. 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: Jaime A Texeira da Silva (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, vol II, 1st edn. Global Science Books™, Isleworth, pp 496-506
29. S Hedhili V Courdavault N Giglioli-Guivarc'h P Gantet 2007 Regulation of the terpene moiety biosynthesis of Catharanthus roseus terpene indole alkaloids Phytochem Rev 6 341 351 10.1007/s11101-006-9021-5
30. A Heyl T Schmulling 2003 Cytokinin signal perception and transduction Curr Opin Plant Biol 6 480 488
31. N Imbault M Thiersault P Dupéron A Benabdelmouna P Doireau 1996 Pravastatin: a tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspension Physiol Plant 98 803 809
32. S Irmler G Schroder B St-Pierre NP Crouch M Hotze J Schmidt D Strack U Matern J Schroder 2000 Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase Plant J 24 797 804
33. CD Johnson SN Chary EA Chernoff Q Zeng MP Running DN Crowell 2005 Protein geranylgeranyltransferase is involved in specific aspects of abscisic acid and auxin signaling in Arabidopsis Plant Physiol 139 722 723 101104/pp105065045
34. D Levêque J Wihlm F Jehl 1996 Pharmacology of Catharanthus alkaloids Bull Cancer 83 176 186
35. S Mahroug V Courdavault M Thiersault B St-Pierre V Burlat 2006 Epidermis is a pivotal site of at least four secondary metabolic pathways in Catharanthus roseus aerial organs Planta 223 1191 1200 10.1007/s00425-005-0167-y
36. S Mahroug V Burlat B St-Pierre 2007 Cellular and sub-cellular organisation of the monoterpenoid indole alkaloid pathway in Catharanthus roseus Phytochem Rev 6 363 381 10.1007/s11101-006-9017-1
37. MG Mason JR Botella 2000 Completing the heterotrimer: isolation and characterization of an Arabidopsis thaliana G protein gamma-subunit cDNA Proc Natl Acad Sci USA 97 14784 14788
38. MG Mason JR Botella 2001 Isolation of a novel G-protein gamma-subunit from Arabidopsis thaliana and its interaction with G beta Biochim Biophys Acta 1520 147 153
39. J Memelink R Verpoorte JW Kijne 2001 ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism Trends Plant Sci 6 212 219
40. FL Menke A Champion JW Kjine J Memelink 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 4455 4463
41. JM Mérillon P Doireau A Guillot JC Chénieux M Rideau 1986 Indole alkaloid accumulation and tryptophan decarboxylase activity in Catharanthus roseus cells cultured in three media Plant Cell Rep 5 23 26
42. TA Morehead BJ Biermann DN Crowell SK Randall 1995 Changes in protein isoprenylation during the growth of suspension-cultured tobacco cells Plant Physiol 109 277 284
43. A Oudin M Courtois M Rideau M Clastre 2007 The iridoid pathway in Catharanthus roseus alkaloid biosynthesis Phytochem Rev 6 259 276 10.1007/s11101-006-9054-9
44. A Oudin S Mahroug V Courdavault N Hervouet C Zelwer M Rodriguez-Concepcion B St-Pierre V Burlat 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 10.1007/s11103-007-9190-7
45. N Papon A Oudin A Vansiri M Rideau JC Chenieux J Crèche 2003 Differential expression of two type-A response regulators in plants and cell cultures of Catharanthus roseus (L.) G. Don J Exp Bot 54 1793 1795
46. N Papon J Bremer A Vansiri F Andreu M Rideau J Crèche 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 10.1055/s-2005-864163
47. ZM Pei M Ghassemian CM Kwak P McCourt JI Schroeder 1998 Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss Science 282 287 290
48. D Qian D Zhou R Ju CL Cramer Z Yang 1996 Protein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control Plant Cell 8 2381 2394
49. Z Ren CE Elson MN Gould 1997 Inhibition of type I and type II geranylgeranyl-protein transferases by the monoterpene perillyl alcohol in NIH3T3 cells Biochem Pharmacol 54 113 120
50. MP Running M Lavy H Sternberg A Galichet W Gruissem S Hake N Ori S Yalovsky 2004 Enlarged meristems and delayed growth in plp mutants results from lack of CaaX-prenyltransferase Proc Natl Acad Sci 101 7815 7820 10.1073/pnas.0402385101
51. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
52. WR Schafer J Rine 1992 Protein prenylation: genes, enzymes, targets and functions Annu Rev Genet 26 209 237
53. T Shoji T Ogawa T Hashimoto 2008 Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ Genes Plant Cell Physiol 49 1003 1012 10.1093/pcp/pcn077
54. M Sinensky 2000 Recent advances in the study of prenylated proteins Biochim Biophys Acta 1484 93 106
55. F Tamanoi 1993 Inhibitors of Ras farnesyltransferases Trends Biochem Sci 18 349 353
56. B Thines L Katsir M Melotto Y Niu A Mandaokar G Liu K Nomura YS He GA Howe J Browse 2007 JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling Nature 448 661 665 10.1038/nature05960
57. Y Trusov JE Rookes D Chakravorty D Armour PM Schenk JR Botella 2006 Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling Plant Physiol 140 210 220 101104/pp105069625
58. Y Trusov JE Rookes K Tilbrook D Chakravorty MG Mason D Anderson J-G Chen AM Jones JR Botella 2007 Heterotrimeric G protein gamma subunits provide functional selectivity in Gβγ dimer signaling in Arabidopsis Plant Cell 19 1235 1250 10.1105/tpc.107.050096
59. L van der Fits J Memelink 2000 ORCA 3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism Science 289 295 297
60. L van der Fits J Memelink 2001 The jasmonate-inducible AP2/ERF-domain transcrition factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element Plant J 25 43 53 10.1046/j.1365-313x.2001. 00932.x
61. B Veau M Courtois A Oudin JC Chenieux M Rideau M Clastre 2000 Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus Biochim Biophys Acta 1517 159 163
62. Y Wang J Ying M Kuzma M Chalifoux A Sample C McArthur T Uchacz C Sarvas J Wan DT Dennis P McCourt Y Huang 2005 Molecular tailoring of farnesylation for plant drought tolerance and yield protection Plant J 43 413 424 10.1111/j.1365-313x.2005.02463.x
63. S Yalovsky A Kulukian M Rodriguez-Conception CA Youg W Gruissem 2000 Functional requirement of plant farnesyltransferase during development in Arabidospsis Plant Cell 12 1267 1278
64. FL Zhang PJ Casey 1996 Protein prenylation: molecular mechanisms and functional consequences Annu Rev Biochem 65 241 269
65. EC Ziegelhoffer LJ Medrano EM Meyerowitz 2000 Cloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development Proc Natl Acad Sci USA 97 7633 7638