The Transcription Factor CrWRKY1 Positively Regulates the Terpenoid Indole Alkaloid Biosynthesis in Catharanthus roseus

Oxford University Press (OUP) - Tập 157 Số 4 - Trang 2081-2093 - 2011
Nitima Suttipanta1,2,3, Sitakanta Pattanaik1,2,3, Mukul Kulshrestha1,2,3, Barunava Patra1,2,3, Sanjay K. Singh1,2,3, Ling Yuan1,2,3
1Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546 (N.S., S.P., L.Y.)
2Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546 (N.S., S.P., L.Y.); Kentucky Tobacco Research and Development Center, Lexington, Kentucky 40546 (S.P., B.P., S.K.S., L.Y.); Naprogenix, Inc., Lexington, Kentucky 40502 (M.K.)
3Naprogenix, Inc., Lexington, Kentucky 40502 (M.K.)

Tóm tắt

Abstract Catharanthus roseus produces a large array of terpenoid indole alkaloids (TIAs) that are an important source of natural or semisynthetic anticancer drugs. The biosynthesis of TIAs is tissue specific and induced by certain phytohormones and fungal elicitors, indicating the involvement of a complex transcriptional control network. However, the transcriptional regulation of the TIA pathway is poorly understood. Here, we describe a C. roseus WRKY transcription factor, CrWRKY1, that is preferentially expressed in roots and induced by the phytohormones jasmonate, gibberellic acid, and ethylene. The overexpression of CrWRKY1 in C. roseus hairy roots up-regulated several key TIA pathway genes, especially Tryptophan Decarboxylase (TDC), as well as the transcriptional repressors ZCT1 (for zinc-finger C. roseus transcription factor 1), ZCT2, and ZCT3. However, CrWRKY1 overexpression repressed the transcriptional activators ORCA2, ORCA3, and CrMYC2. Overexpression of a dominant-repressive form of CrWRKY1, created by fusing the SRDX repressor domain to CrWRKY1, resulted in the down-regulation of TDC and ZCTs but the up-regulation of ORCA3 and CrMYC2. CrWRKY1 bound to the W box elements of the TDC promoter in electrophoretic mobility shift, yeast one-hybrid, and C. roseus protoplast assays. Up-regulation of TDC increased TDC activity, tryptamine concentration, and resistance to 4-methyl tryptophan inhibition of CrWRKY1 hairy roots. Compared with control roots, CrWRKY1 hairy roots accumulated up to 3-fold higher levels of serpentine. The preferential expression of CrWRKY1 in roots and its interaction with transcription factors including ORCA3, CrMYC2, and ZCTs may play a key role in determining the root-specific accumulation of serpentine in C. roseus plants.

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Tài liệu tham khảo

Aerts, 1994, Methyl jasmonate vapor increases the developmentally controlled synthesis of alkaloids in Catharanthus and Cinchona seedlings, Plant J, 5, 635, 10.1111/j.1365-313X.1994.00635.x

Choi, 2004, Plant regeneration from hairy-root cultures transformed by infection with Agrobacterium rhizogenes in Catharanthus roseus, Plant Cell Rep, 22, 828, 10.1007/s00299-004-0765-3

Costa, 2008, Molecular cloning and characterization of a vacuolar class III peroxidase involved in the metabolism of anticancer alkaloids in Catharanthus roseus, Plant Physiol, 146, 403, 10.1104/pp.107.107060

El-Sayed, 2004, Growth, metabolic profiling and enzymes activities of Catharanthus roseus seedlings treated with plant growth regulators, Plant Growth Regul, 44, 53, 10.1007/s10725-004-2604-5

El-Sayed, 2007, Catharanthus terpenoid indole akaloids: biosynthesis and regulation, Phytochem Rev, 6, 277, 10.1007/s11101-006-9047-8

Eulgem, 2000, The WRKY superfamily of plant transcription factors, Trends Plant Sci, 5, 199, 10.1016/S1360-1385(00)01600-9

Facchini, 2008, Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants, Plant J, 54, 763, 10.1111/j.1365-313X.2008.03438.x

Ferreres, 2010, Simple and reproducible HPLC-DAD-ESI-MS/MS analysis of alkaloids in Catharanthus roseus roots, J Pharm Biomed Anal, 51, 65, 10.1016/j.jpba.2009.08.005

Goddijn, 1995, Overexpression of a tryptophan decarboxylase cDNA in Catharanthus roseus crown gall calluses results in increased tryptamine levels but not in increased terpenoid indole alkaloid production, Transgenic Res, 4, 315, 10.1007/BF01972528

Goddijn, 1993, A chimaeric tryptophan decarboxylase gene as a novel selectable marker in plant cells, Plant Mol Biol, 22, 907, 10.1007/BF00027376

Goklany, 2009, Assessing the limitations to terpenoid indole alkaloid biosynthesis in Catharanthus roseus hairy root cultures through gene expression profiling and precursor feeding, Biotechnol Prog, 25, 1289, 10.1002/btpr.204

Hiratsu, 2003, Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis, Plant J, 34, 733, 10.1046/j.1365-313X.2003.01759.x

Hong, 2006, Expression of the Arabidopsis feedback-insensitive anthranilate synthase holoenzyme and tryptophan decarboxylase genes in Catharanthus roseus hairy roots, J Biotechnol, 122, 28, 10.1016/j.jbiotec.2005.08.008

Hughes, 2004, Metabolic engineering of the indole pathway in Catharanthus roseus hairy roots and increased accumulation of tryptamine and serpentine, Metab Eng, 6, 268, 10.1016/j.ymben.2004.03.002

Kato, 2007, Identification of a WRKY protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in Coptis japonica, Plant Cell Physiol, 48, 8, 10.1093/pcp/pcl041

Larkin, 2007, Clustal W and Clustal X version 2.0, Bioinformatics, 23, 2947, 10.1093/bioinformatics/btm404

Liu, 2007, Terpenoid indole alkaloids biosynthesis and metabolic engineering in Catharanthus roseus, J Integr Plant Biol, 49, 961, 10.1111/j.1672-9072.2007.00457.x

Memelink, 2007, Transcription factors involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus, Phytochem Rev, 6, 353, 10.1007/s11101-006-9051-z

Menke, 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, 10.1093/emboj/18.16.4455

Miranda-Ham, 2007, Accumulation of monoterpenoid indole alkaloids in periwinkle seedlings (Catharanthus roseus) as a model for the study of plant-environment interactions, Biochem Mol Biol Educ, 35, 206, 10.1002/bmb.60

Montiel, 2007, Transcription factor Agamous-like 12 from Arabidopsis promotes tissue-like organization and alkaloid biosynthesis in Catharanthus roseus suspension cells, Metab Eng, 9, 125, 10.1016/j.ymben.2006.10.001

Murata, 2006, Expressed sequence tags from Madagascar periwinkle (Catharanthus roseus), FEBS Lett, 580, 4501, 10.1016/j.febslet.2006.07.020

Naoumkina, 2008, Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula, BMC Plant Biol, 8, 132, 10.1186/1471-2229-8-132

O’Connor, 2006, Chemistry and biology of monoterpene indole alkaloid biosynthesis, Nat Prod Rep, 23, 532, 10.1039/b512615k

Ouwerkerk, 1999, Elicitor-responsive promoter regions in the tryptophan decarboxylase gene from Catharanthus roseus, Plant Mol Biol, 39, 129, 10.1023/A:1006138601744

Pattanaik, 2010, Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco, Planta, 231, 1061, 10.1007/s00425-010-1108-y

Pauw, 2004, Zinc finger proteins act as transcriptional repressors of alkaloid biosynthesis genes in Catharanthus roseus, J Biol Chem, 279, 52940, 10.1074/jbc.M404391200

Peebles, 2009, Transcriptional response of the terpenoid indole alkaloid pathway to the overexpression of ORCA3 along with jasmonic acid elicitation of Catharanthus roseus hairy roots over time, Metab Eng, 11, 76, 10.1016/j.ymben.2008.09.002

Ramamoorthy, 2008, A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments, Plant Cell Physiol, 49, 865, 10.1093/pcp/pcn061

Roepke, 2010, Vinca drug components accumulate exclusively in leaf exudates of Madagascar periwinkle, Proc Natl Acad Sci USA, 107, 15287, 10.1073/pnas.0911451107

Runguphan, 2009, Silencing of tryptamine biosynthesis for production of nonnatural alkaloids in plant culture, Proc Natl Acad Sci USA, 106, 13673, 10.1073/pnas.0903393106

Rushton, 2010, WRKY transcription factors, Trends Plant Sci, 15, 247, 10.1016/j.tplants.2010.02.006

Sibéril, 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, 10.1023/A:1010650906695

St-Pierre, 1999, Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate, Plant Cell, 11, 887, 10.1105/tpc.11.5.887

Suttipanta, 2007, Promoter analysis of the Catharanthus roseus geraniol 10-hydroxylase gene involved in terpenoid indole alkaloid biosynthesis, Biochim Biophys Acta, 1769, 139, 10.1016/j.bbaexp.2007.01.006

Tamura, 2007, MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0, Mol Biol Evol, 24, 1596, 10.1093/molbev/msm092

van der Fits, 2000, ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism, Science, 289, 295, 10.1126/science.289.5477.295

van der Fits, 2000, A Catharanthus roseus BPF-1 homologue interacts with an elicitor-responsive region of the secondary metabolite biosynthetic gene Str and is induced by elicitor via a JA-independent signal transduction pathway, Plant Mol Biol, 44, 675, 10.1023/A:1026526522555

Vázquez-Flota, 2009, A differential response to chemical elicitors in Catharanthus roseus in vitro cultures, Biotechnol Lett, 31, 591, 10.1007/s10529-008-9881-4

Vom Endt, 2007, Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-Hook DNA-binding proteins, Plant Physiol, 144, 1680, 10.1104/pp.107.096115

Wang, 2010, Overexpression of G10H and ORCA3 in the hairy roots of Catharanthus roseus improves catharanthine production, Plant Cell Rep, 29, 887, 10.1007/s00299-010-0874-0

Wang, 2010, Isolation and functional analysis of the Catharanthus roseus deacetylvindoline-4-O-acetyltransferase gene promoter, Plant Cell Rep, 29, 185, 10.1007/s00299-009-0811-2

Wei, 2010, Methyl jasmonic acid induced expression pattern of terpenoid indole alkaloid pathway genes in Catharanthus roseus seedlings, Plant Growth Regul, 61, 243, 10.1007/s10725-010-9468-7

Xu, 2006, Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors, Plant Cell, 18, 1310, 10.1105/tpc.105.037523

Yamasaki, 2005, Solution structure of an Arabidopsis WRKY DNA binding domain, Plant Cell, 17, 944, 10.1105/tpc.104.026435

Zhang, 2011, The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus, Plant J, 67, 61, 10.1111/j.1365-313X.2011.04575.x

Zhang, 2005, The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants, BMC Evol Biol, 5, 1, 10.1186/1471-2148-5-1

Zhou, 2009, Production and metabolic engineering of terpenoid indole alkaloids in cell cultures of the medicinal plant Catharanthus roseus (L.) G. Don (Madagascar periwinkle), Biotechnol Appl Biochem, 52, 313, 10.1042/BA20080239

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Oxford University Press (OUP)

Tập 157 Số 4

2081-2093

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