Key points are not available for this paper at this time.
In Catharanthus roseus cell suspensions, the expression of several terpenoid indole alkaloid biosynthetic genes, including two genes encoding strictosidine synthase (STR) and tryptophan decarboxylase (TDC), is coordinately induced by fungal elicitors such as yeast extract. To identify molecular mechanisms regulating the expression of these genes, a yeast one-hybrid screening was performed with an elicitor-responsive part of the TDC promoter. This screening identified three members of the Cys2/His2-type (transcription factor IIIA-type) zinc finger protein family from C. roseus, ZCT1, ZCT2, and ZCT3. These proteins bind in a sequence-specific manner to the TDC and STR promoters in vitro and repress the activity of these promoters in trans-activation assays. In addition, the ZCT proteins can repress the activating activity of APETALA2/ethylene response-factor domain transcription factors, the ORCAs, on the STR promoter. The expression of the ZCT genes is rapidly induced by yeast extract and methyljasmonate. These results suggest that the ZCT proteins act as repressors in the regulation of elicitor-induced secondary metabolism in C. roseus. In Catharanthus roseus cell suspensions, the expression of several terpenoid indole alkaloid biosynthetic genes, including two genes encoding strictosidine synthase (STR) and tryptophan decarboxylase (TDC), is coordinately induced by fungal elicitors such as yeast extract. To identify molecular mechanisms regulating the expression of these genes, a yeast one-hybrid screening was performed with an elicitor-responsive part of the TDC promoter. This screening identified three members of the Cys2/His2-type (transcription factor IIIA-type) zinc finger protein family from C. roseus, ZCT1, ZCT2, and ZCT3. These proteins bind in a sequence-specific manner to the TDC and STR promoters in vitro and repress the activity of these promoters in trans-activation assays. In addition, the ZCT proteins can repress the activating activity of APETALA2/ethylene response-factor domain transcription factors, the ORCAs, on the STR promoter. The expression of the ZCT genes is rapidly induced by yeast extract and methyljasmonate. These results suggest that the ZCT proteins act as repressors in the regulation of elicitor-induced secondary metabolism in C. roseus. Perception of stress signals or of pathogen-derived molecules, called elicitors, activates a number of signal transduction steps in plants, eventually leading to the transcriptional activation of numerous genes, and consequently to de novo synthesis of a variety of defense proteins and protective secondary metabolites (1Nimchuk Z. Eulgem T. Holt B.F. II I Dangl J.F. Annu. Rev. Genet. 2003; 37: 579-609Crossref PubMed Scopus (441) Google Scholar). The biosynthesis of one or more secondary signals, such as jasmonic acid (JA), 1The abbreviations used are: JA, jasmonic acid; MeJA, methyljasmonate; BPF, box P-binding factor; GBF, G-box-binding factor; YE, yeast extract; STR, strictosidine synthase; TDC, tryptophan decarboxylase; ORCA, octadecanoid-responsive Catharanthus AP2 domain; AP2, APETALA2; ERF, ethylene-response-factor; TFIIIA, transcription factor IIIA; EMSA, electrophoretic mobility shift assay; GUS, β-glucuronidase; ZCT, zinc finger Catharanthus transcription factor. salicylic acid, and ethylene, plays a crucial role in this stress response (2Kunkel B.N. Brooks D.M. Curr. Opin. Plant Biol. 2002; 5: 325-331Crossref PubMed Scopus (1160) Google Scholar). In elicitor-induced accumulation of secondary metabolites, jasmonic acid and its volatile methyl-ester methyljasmonate (MeJA), have been shown to act as intermediate signals (3Memelink J. Verpoorte R. Kijne J.W. Trends Plant Sci. 2001; 6: 212-219Abstract Full Text Full Text PDF PubMed Scopus (286) Google Scholar). Knowledge about the molecular mechanisms regulating elicitor-responsive expression of secondary metabolite biosynthesis genes is limited. In parsley, a fungal elicitor induces the expression of the MYB-like transcription factor box P-binding factor (BPF)-1, which interacts with the promoter of a gene encoding the phenylpropanoid biosynthesis enzyme phenylalanine ammonia-lyase (4da Costa e Silva O. Klein L. Schmelzer E. Trezzini G.F. Hahlbrock K. Plant J. 1993; 4: 125-135Crossref PubMed Scopus (82) Google Scholar). Terpenoid indole alkaloid biosynthesis in Catharanthus roseus is one of the best studied elicitor-induced secondary metabolic pathways. In suspension cells, the perception of yeast extract (YE) leads to the activation of terpenoid indole alkaloid biosynthesis (5Moreno P.R.H. van der Heijden R. Verpoorte R. Plant Cell Tissue Org. Cult. 1995; 42: 1-25Crossref Scopus (202) Google Scholar). Two genes involved in terpenoid indole alkaloid biosynthesis, encoding strictosidine synthase (STR) and tryptophan decarboxylase (TDC), are coordinately regulated and their mRNAs accumulate transiently after YE treatment (6Pasquali G. Goddijn O.J.M. de Waal A. Verpoorte R. Schilperoort R.A. Hoge J.H.C. Memelink J. Plant Mol. Biol. 1992; 18: 1121-1131Crossref PubMed Scopus (197) Google Scholar, 7Roewer I.A. Cloutier C. Nessler C.L. De Luca V. Plant Cell Rep. 1992; 11: 86-89Crossref PubMed Scopus (49) Google Scholar). Induction of these genes by YE is mediated by protein phosphorylation, the influx of calcium, and the biosynthesis of JA via the octadecanoid pathway (3Memelink J. Verpoorte R. Kijne J.W. Trends Plant Sci. 2001; 6: 212-219Abstract Full Text Full Text PDF PubMed Scopus (286) Google Scholar, 8Menke F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google Scholar). In the STR promoter, two elicitor- and jasmonate-responsive sequences have been identified; the so-called BA region and a sequence close to the TATA box, called jasmonate- and elicitor-responsive element, located in the RV region (see Fig. 8). The BA region was found to bind to a homologue of parsley PcBPF-1, called CrBPF1 (9van der Fits L. Zhang H. Menke F.L.H. Deneka M. Memelink J. Plant Mol. Biol. 2000; 44: 675-685Crossref PubMed Scopus (111) Google Scholar). The jasmonate- and elicitor-responsive element interacts with two JA-responsive transcription factors called ORCA2 and ORCA3 (10Menke F.L.H. Champion A. Kijne J.W. Memelink J. EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google Scholar, 11van der Fits L. Memelink J. Plant J. 2001; 25: 43-53Crossref PubMed Google Scholar). Both ORCAs belong to the APETALA2/ethylene response-factor (AP2/ERF) family of transcription factors. ORCA3 was shown to regulate multiple genes involved in primary and secondary metabolism, including the TDC and STR genes (3Memelink J. Verpoorte R. Kijne J.W. Trends Plant Sci. 2001; 6: 212-219Abstract Full Text Full Text PDF PubMed Scopus (286) Google Scholar, 11van der Fits L. Memelink J. Plant J. 2001; 25: 43-53Crossref PubMed Google Scholar, 12van der Fits L. Memelink J. Science. 2000; 289: 295-297Crossref PubMed Scopus (764) Google Scholar). The NR region of the STR promoter, which is not required for responsiveness to elicitor or jasmonate (10Menke F.L.H. Champion A. Kijne J.W. Memelink J. EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google Scholar), interacts with two G-box proteins S. Memelink J. M. Plant Mol. Biol. 2001; PubMed Scopus Google Scholar). The TDC promoter a element, the so-called element Memelink J. Plant Mol. Biol. 1999; PubMed Scopus Google Scholar). The transcription factors or the protein CrBPF1 (9van der Fits L. Zhang H. Menke F.L.H. Deneka M. Memelink J. Plant Mol. Biol. 2000; 44: 675-685Crossref PubMed Scopus (111) Google not bind to the element, have a for a sequence in the element in vitro S. Memelink J. M. Plant Mol. Biol. 2001; PubMed Scopus Google Scholar). To transcription factors that with the element, a yeast one-hybrid screening was This screening identified three members of the transcription factor zinc finger protein family from C. roseus, ZCT1, ZCT2, and ZCT3. In vitro that these proteins bind in a sequence-specific manner to the TDC and STR these zinc finger proteins shown to act as transcriptional repressors of STR and TDC promoter activity in trans-activation assays. expression of these zinc finger genes is rapidly induced by YE and these that zinc finger transcription factors can act as repressors in the regulation of secondary of encoding zinc finger proteins ZCT1, ZCT2, and by a one-hybrid screening of a C. roseus with the element of the TDC promoter as of the element from the TDC promoter was in Memelink J. Plant Mol. Biol. 1999; PubMed Scopus Google Scholar). The was to the yeast gene in S. C. Science. 1992; PubMed Scopus Google Scholar). The was as a the of which is to Hoge J.H.C. PubMed Scopus (49) Google Scholar). The was with and yeast J.W. K. 1993; Full Text PDF PubMed Scopus Google Scholar). on and the of the and the was by The with a of was from C. roseus cell suspension as by F.L.H. Champion A. Kijne J.W. Memelink J. EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google of the the yeast on and of an number of yeast in and of members of in the of three zinc finger of sequences by with a and the the as a to a To this sequences with the with and in of the sequence of sequences with the with and in The from the was with and the M. PubMed Scopus Google with after which was as a to the the with in a sequences with the with and in The from the was with and the after which was as a to the the in a of was from the with and in with The was used as with and in a and the was with and in was with and in PubMed Scopus Google Scholar). The was with the and and after with was in The was with the and and with in in E. and proteins to the electrophoretic mobility shift promoter RV and (10Menke F.L.H. Champion A. Kijne J.W. Memelink J. EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google Scholar), and TDC promoter Memelink J. Mol. Genet. 1999; PubMed Scopus Google and as of of and protein extract in a of the of zinc for ZCT proteins for in or of for on for on and of Plant was from with in with and in as a The was from with and in The are a promoter and the by a The was as a in This a promoter and the by a Cell roseus cell suspension was as (6Pasquali G. Goddijn O.J.M. de Waal A. Verpoorte R. Schilperoort R.A. Hoge J.H.C. Memelink J. Plant Mol. Biol. 1992; 18: 1121-1131Crossref PubMed Scopus (197) Google Scholar). of C. roseus cell with promoter to and ZCT1, ZCT2, ORCA2 or ORCA3 to the promoter. of the with an as with a of of as der Fits L. Memelink J. Plant Mol. Biol. PubMed Scopus Google Scholar), the two in a of In the of with and zinc finger the was was in of an of after and in activity performed as der Fits L. Memelink J. Plant Mol. Biol. PubMed Scopus Google Scholar). activity was to protein to for the of used in activity was as activity with the of the results was the and elicitor was from yeast extract (YE) and a number of as in 8Menke F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google The of elicitor used for was to to a of of YE a response as F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google Scholar). was in and and performed as F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google Scholar), the and STR F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google Scholar). of ZCT1, ZCT2, and identify proteins that with the element of the TDC promoter, a yeast one-hybrid screening was performed with this of yeast a of to the was used in a to proteins from a of C. roseus in a with the activation domain in yeast expression In for gene of to several from yeast that on encoding or CrBPF1 proteins which is with the that these proteins not bind in In addition, encoding the that have a for a sequence in the element in vitro S. Memelink J. M. Plant Mol. Biol. 2001; PubMed Scopus Google Scholar). of the sequences to sequences in the that three proteins with two Cys2/His2-type zinc In a zinc finger two and two in a sequence a zinc to a that interacts with the of in a sequence-specific manner C. Science. PubMed Scopus Google Scholar, A. Curr. Opin. Biol. PubMed Scopus Google Scholar). three Catharanthus the of proteins H. Plant Mol. Biol. 1999; PubMed Scopus Google Scholar). Both have the sequence in the and the two are by a called the three proteins ZCT1, ZCT2, and for zinc finger Catharanthus transcription factor. The was the and was a The from the was and to The of and via and to the to of the acid sequences of ZCT1, ZCT2, and is shown in Fig. The ZCT1, ZCT2, and proteins have molecular of and of the and acid sequences to sequences in the to and from of the of is the protein from which is involved in M.J. Plant J. 2001; 25: PubMed Google Scholar). the two zinc the ZCT proteins several their a region H. T. T. M. 2000; PubMed Scopus Google Scholar), which as a signal the and the zinc the ZCT proteins a region of in The been found in several zinc finger and been to a role in or in the of the proteins H. T. T. M. 2000; PubMed Scopus Google Scholar, R. Plant Mol. Biol. PubMed Scopus Google Scholar). In their the ZCT proteins have an which is a domain found in zinc several M. K. K. H. M. Plant 2001; PubMed Scopus Google Scholar), and in G. Plant PubMed Scopus Google transcriptional In proteins this been called the domain M. K. K. H. M. Plant 2001; PubMed Scopus Google Scholar). The ZCT to of the TDC and STR of the ZCT proteins to gene expression via the region in yeast and the of two zinc finger that are To the of the zinc finger proteins from E. and of the ZCT proteins with from the TDC promoter that can bind to this and a of two a To the ZCT proteins can bind to of the TDC promoter, performed with a region of the TDC promoter of the TATA box and with to the and of the TDC promoter, with to the to of the TDC promoter with for and not bind to of the used in not the TDC and STR genes are coordinately regulated by YE and MeJA, the of the ZCT proteins to the STR promoter was of the zinc finger in to a yeast a of the RV region of the STR promoter to the gene (10Menke F.L.H. Champion A. Kijne J.W. Memelink J. 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EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google Scholar), that the is located in the To the of the ZCT proteins in the RV the RV used as in the ZCT proteins or to RV bind to the RV can that the for the ZCT proteins is located in the region The ZCT is from with the for the To the of the ZCT proteins with the of a zinc to their zinc the of the ZCT proteins was in the of the or Fig. that the ZCT proteins can bind to the RV the of or the of the ZCT proteins to the RV that zinc is required for The of which a to calcium, or the not the of the ZCT proteins to RV the of the by and the of the TDC promoter that zinc is for the of the ZCT proteins to this not The ZCT as of STR and TDC of the zinc finger proteins to the TDC and STR promoters that these proteins involved in the regulation of the expression of these To the ZCT proteins can regulate these promoters in C. roseus with a and an a ZCT to the promoter. of of the ZCT proteins TDC promoter activity with the of of the ZCT proteins STR promoter activity These results that the ZCT proteins can act as transcriptional repressors of the TDC and STR The activity of the ZCT proteins is with the of the these in on the STR promoter, its with to and their with factors been in more for the TDC promoter Memelink J. 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Both and ZCT repressors can bind to the RV element of the STR promoter. proteins the transcriptional activity of the RV was not by the ZCT the transcriptional activity of a STR promoter was by the ZCT proteins proteins This that in the promoter the ZCT proteins STR promoter activity via to the BA in a is that and ZCT proteins have expression a as is by the of and ZCT accumulation in response to YE and This to about the in and these proteins In perception of YE activates the octadecanoid which leads to an in JA F.L.H. Parchmann S. Mueller M.J. Kijne J.W. Memelink J. Plant Physiol. 1999; 119: 1289-1296Crossref PubMed Scopus (214) Google Scholar). JA induces the expression of the genes, the ORCA3 and activates proteins via der Fits L. Memelink J. Plant J. 2001; 25: 43-53Crossref PubMed Google Scholar). The proteins can gene expression via with the TDC promoter and the and JA-responsive RV of the STR promoter F.L.H. Champion A. Kijne J.W. Memelink J. EMBO J. 1999; 18: 4455-4463Crossref PubMed Scopus (370) Google Scholar, 11van der Fits L. Memelink J. Plant J. 2001; 25: 43-53Crossref PubMed Google Scholar, 12van der Fits L. Memelink J. Science. 2000; 289: 295-297Crossref PubMed Scopus (764) Google Scholar). In addition, YE rapidly induces the expression of the zinc finger proteins which can repress gene expression via to the of the TDC promoter and the and JA-responsive BA and RV of the STR promoter 8). YE induces accumulation of encoding which is involved in the regulation of STR via with the BA region (9van der Fits L. Zhang H. Menke F.L.H. Deneka M. Memelink J. Plant Mol. Biol. 2000; 44: 675-685Crossref PubMed Scopus (111) Google Scholar). transcription factors can repress STR promoter activity via to the NR region S. Memelink J. M. Plant Mol. Biol. 2001; PubMed Scopus Google Scholar). 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