Abstract
CaaX-prenyltransferases (CaaX-PTases) catalyse the covalent attachment of isoprenyl groups to conserved cysteine residues located at the C-terminal CaaX motif of a protein substrate. This post-translational modification is required for the function and/or subcellular localization of some transcription factors and components of signal transduction and membrane trafficking machinery. CaaX-PTases, including protein farnesyltransferase (PFT) and type-I protein geranylgeranyltransferase (PGGT-I), are heterodimeric enzymes composed of a common α subunit and a specific β subunit. We have established RNA interference cell lines targeting the β subunits of PFT and PGGT-I, respectively, in the Catharanthus roseus C20D cell line, which synthesizes monoterpenoid indole alkaloids in response to auxin depletion from the culture medium. In both types of RNAi cell lines, expression of a subset of genes involved in the early stage of monoterpenoid biosynthetic pathway (ESMB genes), including the MEP pathway, is strongly decreased. The role of CaaX-PTases in ESMB gene regulation was confirmed by using the general prenyltransferase inhibitor s-perillyl alcohol (SP) and the specific PFT inhibitor Manumycin A on the wild type line. Furthermore, supplementation of SP inhibited cells with monoterpenoid intermediates downstream of the steps encoded by the ESMB genes restores monoterpenoid indole alkaloids biosynthesis. We conclude that protein targets for both PFT and PGGT-I are required for the expression of ESMB genes and monoterpenoid biosynthesis in C. roseus, this represents a non previously described role for protein prenyltransferase in plants.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- ESMB genes:
-
early stages of monoterpenoid biosynthetic pathway genes
- MIA:
-
monoterpenoid indole alkaloids
- MM:
-
maintenance medium
- PFT:
-
protein farnesyltransferase
- PGGT-I:
-
type-I protein geranylgeranyltransferase
- PM:
-
production medium
- PPT:
-
protein- prenyltransferase
References
M.P. Arvy N. Imbault F. Naudascher M. Thiersault P Doireau (1994) ArticleTitle2,4-D and alkaloid accumulation in periwinkle cell suspensions Biochimie 76 410–416 Occurrence Handle10.1016/0300-9084(94)90117-1 Occurrence Handle1:CAS:528:DyaK2MXitVKqur4%3D Occurrence Handle7849107
T.J Bach (1995) ArticleTitleSome new aspects of isoprenoid biosynthesis in plants Lipids 30 191–202 Occurrence Handle1:CAS:528:DyaK2MXks1KqurY%3D Occurrence Handle7791527
V. Burlat A. Oudin M. Courtois M. Rideau B St-Pierre (2004) ArticleTitleCo-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 Occurrence Handle10.1111/j.1365-313X.2004.02030.x Occurrence Handle1:CAS:528:DC%2BD2cXktVOiu7w%3D Occurrence Handle15053766
D. Caldelari H. Sternberg M. Rodriguez-Concepcion W. Gruissem S Yalovsky (2001) ArticleTitleEfficient prenylation by a plant geranylgeranyltransferase-I requires a functional CaaL box motif and a proximal polybasic domain Plant Physiol. 126 1416–1429 Occurrence Handle10.1104/pp.126.4.1416 Occurrence Handle1:CAS:528:DC%2BD3MXlvFOjurw%3D Occurrence Handle11500541
P.J Casey (1995) ArticleTitleProtein lipidation in cell signalling Science 268 221–225 Occurrence Handle1:CAS:528:DyaK2MXltVCitLs%3D Occurrence Handle7716512
P.J. Casey P.A. Solski C.J. Der J.E Buss (1989) ArticleTitlep21ras is modified by a farnesyl isoprenoid Proc. Natl. Acad. Sci. USA 86 8323–8327 Occurrence Handle1:CAS:528:DyaK3cXltVOitA%3D%3D Occurrence Handle2682646
K. Chahed A. Oudin N. Guivarc’h S. Hamdi J.-C. Chénieux M. Rideau M Clastre (2000) ArticleTitle1-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 Occurrence Handle10.1016/S0981-9428(00)00781-6 Occurrence Handle1:CAS:528:DC%2BD3cXms1GjtLo%3D
J. Chappell (2002) ArticleTitleThe genetics and molecular genetics of terpene and sterol origami Curr. Opin. Plant Biol. 5 151–157 Occurrence Handle10.1016/S1369-5266(02)00241-8 Occurrence Handle1:CAS:528:DC%2BD38XhtlGnsbk%3D Occurrence Handle11856612
A. Contin R. Heijden A.W.M. Lefeber R Verpoort (1998) ArticleTitleThe iridoid glucoside secologanin is derived from the novel triose phosphate/pyruvate pathway in a Catharanthus roseus cell culture FEBS Lett. 437 413–416
V. Courdavault V. Burlat B. St-Pierre (2005) ArticleTitleGiglioli-Guivarc’h,N. 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 Occurrence Handle1:CAS:528:DC%2BD2MXhslWnsLg%3D
P.L. Crowell Z. Ren S. Lin E. Vedejs M.N Gould (1994) ArticleTitleStructure-activity relationships among monoterpene inhibitors of protein isoprenylation and cell proliferation Biochem. Pharmacol. 47 1405–1415 Occurrence Handle1:CAS:528:DyaK2cXjtFGhsr4%3D Occurrence Handle8185648
S. Cutler M. Ghassemian D. Bonetta S. Cooney P McCourt (1996) ArticleTitleA protein farnesyltransferase involved in abscisic acid signal transduction in Arabidopsis Science 273 1239–1241 Occurrence Handle1:CAS:528:DyaK28Xltlajs74%3D Occurrence Handle8703061
S.L. Dellaporta J. Wood J.B Hicks (1983) ArticleTitleA plant DNA minipreparation, Version II Plant Mol. Biol. Rep. 1 19–21 Occurrence Handle1:CAS:528:DyaL2cXksFWhtrk%3D
C.C. Farnsworth M.H. Gelb J.A Glomset (1990) ArticleTitleIdentification of geranylgeranyl-modified proteins in HeLa cells Science 247 320–322 Occurrence Handle1:CAS:528:DyaK3cXhtlCkt74%3D Occurrence Handle2296721
O.L. Gamborg R.R.A. Miller K Ojima (1968) ArticleTitleNutriment requirements of suspension cultures of soybean root cells Exp. Cells Res. 50 151–158 Occurrence Handle1:CAS:528:DyaF1cXktVyqtLw%3D
M.H. Gelb F. Tamanoi K. Yokoyama F. Ghomashchi K. Esson M.N Gould (1995) ArticleTitleThe inhibition of protein prenyltransferases by oxygenated metabolites of limonene and perillyl alcohol Cancer Lett. 91 169–175 Occurrence Handle1:CAS:528:DyaK2MXlvVSqs70%3D Occurrence Handle7767906
J.B. Gibbs D.L. Pompliano S.D. Mosser E. Rands R.B. Lingham S.B. Singh E.M. Scolnick N.E. Kohl A Oliff (1993) ArticleTitleSelective inhibition of farnesyl-protein transferase blocks ras processing in vivo J. Biol. Chem. 268 7617–7620 Occurrence Handle1:CAS:528:DyaK3sXks1yktrk%3D Occurrence Handle8463291
J.L Giner (1998) ArticleTitleNew and efficient synthetic routes to 1-Deoxy-D-xylulose Tetrahedron Lett. 39 2479–2482 Occurrence Handle1:CAS:528:DyaK1cXisFOgsr8%3D
J.A. Glomset M.H. Gelb C.C Farnsworth (1990) ArticleTitlePrenyl proteins in eucaryotic cells: a new type of membrane anchor Trends Biochem. Sci. 15 139–142 Occurrence Handle1:CAS:528:DyaK3cXksFCgu70%3D Occurrence Handle2187294
M. Hara K. Akasaka S. Akinaga M. Okabe H. Nakano R. Gomez D. Wood M. Uh F Tamanoi (1993) ArticleTitleIdentification of Ras farnesyltransferase inhibitors by microbial screening Proc. Natl. Acad. Sci. USA 90 2281–2285 Occurrence Handle1:CAS:528:DyaK3sXksVSgu7k%3D Occurrence Handle8460134
K. Haralampidis G. Bryan X. Qi K. Papadopoulou S. Bakht R. Melton A Osbourn (2001) ArticleTitleA new class of oxidosqualene cyclases directs synthesis of antimicrobial phytoprotectants in monocots Proc. Natl. Acad. Sci. USA 98 13431–13436 Occurrence Handle1:CAS:528:DC%2BD3MXosFyguro%3D Occurrence Handle11606766
N. Imbault M Thiersault P. Dupéron A. Benabdelmouna P Doireau (1996) ArticleTitlePravastatine: a tool for investigating the availability of mevalonate metabolites for primary and secondary metabolism in Catharanthus roseus cell suspensions Physiol. Plant 98 803–809 Occurrence Handle1:CAS:528:DyaK2sXhsFyhsA%3D%3D
S Irmler G. Schroder B. St-Pierre N.P. Crouch M. Hotze J. Schmidt D. Strack U. Matern J Schroder (2000) ArticleTitleIndole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase Plant J. 24 797–804 Occurrence Handle1:CAS:528:DC%2BD3MXhtVCht7Y%3D Occurrence Handle11135113
Y. Iwasaki Y. Fujisawa H Kato (2003) ArticleTitleFunction of Heterotrimeric G Protein in Gibberellin Signalling J. Plant Growth Regul. 22 126–133 Occurrence Handle1:CAS:528:DC%2BD3sXovV2lu7w%3D
H. Kasahara A. Hanada T. Kuzuyama M. Takagi Y. Kamiya S Yamaguchi (2002) ArticleTitleContribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis J. Biol. Chem. 277 45188–45194 Occurrence Handle1:CAS:528:DC%2BD38Xosl2lsL4%3D Occurrence Handle12228237
A. Kessler I.T Baldwin (2001) ArticleTitleDefensive function of herbivore-induced plant volatile emissions in nature Science 291 2141–2144 Occurrence Handle1:CAS:528:DC%2BD3MXitFCltr0%3D Occurrence Handle11251117
D. Levêque J. Wihlm F Jehl (1996) ArticleTitlePharmacology of Catharanthus alkaloids Bull. Cancer 83 176–186 Occurrence Handle8695919
H.K. Lichtenthaler J. Schwender A. Disch M Rhomer (1997) ArticleTitleBiosynthesis of isoprenoids in higher plant chloroplasts proceeds via a so far unexpected novel pathway FEBS Lett. 400 271–274 Occurrence Handle1:CAS:528:DyaK2sXktl2gug%3D%3D Occurrence Handle9009212
H.K Lichtenthaler (1999) ArticleTitleThe 1-deoxy-D-xylulose 5-phosphate pathway of isoprenoid biosynthesis in plants Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 47–65 Occurrence Handle1:CAS:528:DyaK1MXkt1yksLo%3D Occurrence Handle15012203
J.M. Mérillon I. Ouelhazi P. Doireau A. Guillot J.C. Chenieux M Rideau (1986) ArticleTitleIndol alkaloid accumulation and tryptophan decarboxylase activity in Catharanthus roseus cells cultured in three different media Plant Cell Rep. 5 23–26
F. Naudascher P. Doireau A. Guillot C. Viel M Thiersault (1989) ArticleTitleTime-course studies on the use of secologanin by Catharanthus roseus cells cultured in vitro J. Plant Physiol. 134 608–612 Occurrence Handle1:CAS:528:DyaL1MXkvFequrY%3D
S. Pandey S.M Assmann (2004) ArticleTitleThe Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein α subunit GPA1 and regulates abscisic acid signalling Plant Cell 16 1616–1632 Occurrence Handle1:CAS:528:DC%2BD2cXlsFWlsbk%3D Occurrence Handle15155892
Papon N., Bremer J., Vansiri A., Andreu F., Rideau M. and Crèche J. Cytokinin and ethylene control indole alkaloid production at the level of the MEP/terpenoid pathway in Catharanthus roseus suspension cells. Planta Med. In press
N. Papon A. Vansiri P. Gantet J.C. Chénieux M. Rideau J Crèche (2004) ArticleTitleHistidine-containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in Catharanthus roseus suspension cells FEBS Lett. 558 85–88 Occurrence Handle1:CAS:528:DC%2BD2cXpsV2gug%3D%3D Occurrence Handle14759521
Z.M. Pei M. Ghassemian C.M. Kwak P. Mc Court J.I Schoerder (1998) ArticleTitleRole of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss Science 282 287–290 Occurrence Handle9765153
D. Qian G. Zhou R. Ju C.L. Cramer Z Yang (1996) ArticleTitleProtein farnesyltransferase in plants: molecular characterization and involvement in cell cycle control Plant Cell 8 2381–2394 Occurrence Handle1:CAS:528:DyaK2sXivVWiuw%3D%3D Occurrence Handle8989889
Z. Ren C.E. Elson M.N Gould (1997) ArticleTitleInhibition of type I and type II geranylgeranyl-protein transferases by the monoterpene perillyl alcohol in NIH3T3 cells Biochem. Pharmacol. 54 113–120 Occurrence Handle1:CAS:528:DyaK2sXlsVGqu74%3D Occurrence Handle9296357
Z. Ren M.N Gould (1994) ArticleTitleInhibition of ubiquinone and cholesterol synthesis by the monoterpene perillyl alcohol Cancer Lett. 76 185–90 Occurrence Handle1:CAS:528:DyaK2cXis1Sktbk%3D Occurrence Handle8149348
E.M. Repko W.A Maltese (1989) ArticleTitlePost-translational isoprenylation of cellular proteins is altered in response to mevalonate availability J. Biol. Chem. 264 9945–9952 Occurrence Handle1:CAS:528:DyaL1MXksFClsLo%3D Occurrence Handle2722887
M. Rodriguez-Concepcion S. Yalovsky M. Zik H. Fromm W Gruissem (1999) ArticleTitleThe prenylation status of a novel plant calmodulin directs plasma membrane or nuclear localization of the protein EMBO J. 18 1996–2007 Occurrence Handle1:CAS:528:DyaK1MXivVyksL4%3D Occurrence Handle10202162
M. Rodriguez-Concepcion G. Toledo-Ortiz S. Yalovsky D. Caldelari W Gruissem (2000) ArticleTitleCarboxyl-methylation of prenylated calmodulin CaM53 is required for efficient plasma membrane targeting of the protein Plant J. 24 775–784 Occurrence Handle1:CAS:528:DC%2BD3MXhtVCht7g%3D Occurrence Handle11135111
M.P. Running M. Lavy H. Sternberg A. Galichet W. Gruissem S. Hake N. Ori S Yalosky (2004) ArticleTitleEnlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases Proc. Natl. Acad. Sci. USA 101 7815–7820 Occurrence Handle1:CAS:528:DC%2BD2cXktlOksro%3D Occurrence Handle15128936
J. Sambrook E.F. Fritsch T. Maniatis (1989) Molecular Cloning: A Laboratory Manual, Ed 2 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
B. St-Pierre F.A. Vazquez-Flota V De Luca (1999) ArticleTitleMulticellular compartimentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate Plant Cell 11 887–900 Occurrence Handle1:CAS:528:DyaK1MXjvVajs7w%3D Occurrence Handle10330473
F Tamanoi (1993) ArticleTitleInhibitors of Ras farnesyltransferases Trends Biochem Sci 8 349–353
L.Z. Tao A.Y. Cheung H.M Wu (2002) ArticleTitlePlant Rac-Like GTPases are activated by auxin and mediate auxin-responsive gene expression Plant Cell 14 2745–2760 Occurrence Handle1:CAS:528:DC%2BD38XovF2qur4%3D Occurrence Handle12417698
H. Ullah J.G. Chen B. Temple D.C. Boyes J.M. Alonso K.R. Davis J.R. Ecker A.M Jones (2003) ArticleTitleThe beta-subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes Plant Cell 15 393–409 Occurrence Handle1:CAS:528:DC%2BD3sXhtlOmtb0%3D Occurrence Handle12566580
O. Van Telligen J.H.M. Sips J.H. Beijnen A. Bult W.J Nooijen (1992) ArticleTitlePharmacology, bio-analysis and pharmacokinetics in the Vinca alkaloids and semi-synthetic derivatives Anticancer Res. 12 1699–1716 Occurrence Handle1444238
B. Veau M. Courtois A. Oudin J.C. Chénieux M. Rideau M Clastre (2000) ArticleTitleCloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus Biochim. Biophys. Acta 1517 159–163 Occurrence Handle1:CAS:528:DC%2BD3cXoslGmsLs%3D Occurrence Handle11118631
M.H. Walter J. Hans D Strack (2002) ArticleTitleTwo distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots Plant J. 31 243–254 Occurrence Handle1:CAS:528:DC%2BD38XntFelsL0%3D Occurrence Handle12164805
S.V. Wesley C.A. Helliwell N.A. Smith M.B. Wang D.T. Rouse Q. Liu P.S. Gooding S.P. Singh D. Abbott P.A. Stoutjesdijk S.P. Robinson A.P. Gleave A.G. Green P.M Waterhouse (2001) ArticleTitleConstruct design for efficient, effective and high-throughput gene silencing in plants Plant J. 27 581–590
Wink M. 1999. Introduction: biochemistry, role and biotechnology of secondary metabolites. In: M. Wink (Ed), Biochemistry of plant secondary metabolism Vol. 2, Sheffield Academic Press and CRC Press, Annual Plant Reviews, pp. 1–16
S. Yalovsky M. Rodriguez-Concepcion K. Bracha G. Toledo-Ortiz W Gruissem (2000a) ArticleTitlePrenylation of the floral transcription factor APETALA1 modulates its function Plant Cell 12 1257–1266 Occurrence Handle1:CAS:528:DC%2BD3cXmsVyjs7k%3D
S. Yalovsky A. Kulukiam M. Rodriguez-Concepcion C.A. Young W Gruissem (2000b) ArticleTitleFunctional requirement of plant farnesyltransferase during development in Arabidopsis Plant Cell 12 1267–1278 Occurrence Handle1:CAS:528:DC%2BD3cXmsVyjs7Y%3D
Y. Yang J. Shah D.F Klessing (1997) ArticleTitleSignal perception and transduction in plant defense responses Genes Dev. 11 1621–1639 Occurrence Handle1:CAS:528:DyaK2sXks1yms7s%3D Occurrence Handle9224713
Z. Yang C.L. Cramer J. Watson (1993) ArticleTitleProtein farnesyltransferase in plants. Molecular cloning and expression of a homolog of the beta subunit from the garden Pea Plant Physiol. 101 667–674 Occurrence Handle1:CAS:528:DyaK3sXkt1emurY%3D Occurrence Handle8278509
Z.L. Zheng Z Yang (2000) ArticleTitleThe Rop GTPase: an emerging signalling switch in plants Plant Mol. Biol. 44 1–9 Occurrence Handle1:CAS:528:DC%2BD3cXotlaju74%3D Occurrence Handle11094975
F.L. Zhang P.J Casey (1996) ArticleTitleProtein prenylation: molecular mechanisms and functional consequences Annu. Rev. Biochem. 65 241–269 Occurrence Handle1:CAS:528:DyaK28XktFamtL0%3D Occurrence Handle8811180
E.C. Ziegelhoffer L.J. Medrano E.M Meyerowitz (2000) ArticleTitleCloning of the Arabidopsis WIGGUM gene identifies a role for farnesylation in meristem development Proc. Natl. Acad. Sci. USA 97 7633–7638 Occurrence Handle1:CAS:528:DC%2BD3cXksVKhsbk%3D Occurrence Handle10840062
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Courdavault, V., Thiersault, M., Courtois, M. et al. CaaX-prenyltransferases are essential for expression of genes involvedin the early stages of monoterpenoid biosynthetic pathwayin Catharanthus roseus cells. Plant Mol Biol 57, 855–870 (2005). https://doi.org/10.1007/s11103-005-3095-0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-005-3095-0