Abstract
Jasmonates and nitric oxide (NO) play important roles in the regulation of the signaling network leading to the biosynthesis of plant secondary metabolites. In this work, we explore the effect of constitutive overexpression of CrORCA3 (octadecanoid-responsive Catharanthus AP2/ERF domain), methyl jasmonate (MeJA), and sodium nitroprusside (SNP) on the differentiated tissue of Catharanthus roseus hairy roots. The changes in catharanthine concentration and in the levels of mRNA transcripts of pathway genes and regulators were tracked for 192 h. ORCA3 overexpression led to a slight decrease of the accumulation of catharanthine, while MeJA treatment caused a large increase in the levels of transcripts of pathway genes and the catharanthine concentration. SNP treatment alone or SNP in combination with MeJA treatment caused a dramatic decrease of the cathanranthine concentration, while at the same time the levels of transcripts of zinc finger-binding proteins genes (ZCTs) increased. The latter treatment also caused a decrease of the levels of transcripts of type-I protein prenyltransferase gene (PGGT-I). This response of transcriptional repressors and pathway genes may explain the antagonistic effects of NO and MeJA on catharanthine biosynthesis in C. roseus hairy roots.
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References
Canel C, Lopes-Cardoso MI, Whitmer S, van der Fits L, Pasquali G, van der Heijden R, Hoge JH, Verpoorte R (1998) Effects of overexpression of strictosidine synthase and tryptophan decarboxylase on alkaloid production by cell cultures of Catharanthus roseus. Planta 205:414–419
Courdavault V, Burlat V, St-Pierre B, Giglioli-Guivarc’h N (2008) 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 Rep 28:83–93
El-Sayed M, Verpoorte R (2007) Catharanthus terpenoid indole alkaloids: biosynthesis and regulation. Phytochem Rev 6:277–305
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Expl Cell Res 50:151–158
Georgiev MI, Pavlov AI, Bley T (2007) Hairy root type plant in vitro systems as sources of bioactive substances. Appl Microbiol Biotechnol 74:1175–1185
Georgiev MI, Weber J, Maciuk A (2009) Bioprocessing of plant cell cultures for mass production of targeted compounds. Appl Microbiol Biotechnol 83:809–823
Horsch RB, Fry J, Hoffmann N, Neidermeyer J, Rogers SG, Fraley RT (1989) Plant molecular biology manual. Kluwer, Dordrecht
Meehan TD, Coscia CJ (1973) Hydroxylation of geraniol and nerol by a monooxygenase from Vinca rosea. Biochem Biophys Res Commun 53:1043–1048
Memelink J, Verpoorte R, Kijne W (2001) ORCAnization of jasmonate-responsive gene expression in alkaloid metabolism. Trends Plant Sci 6:212–219
Menke FL, Parchmann S, Mueller MJ, Kijne JW, Memelink J (1999) Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthetic genes in Catharanthus roseus. Plant Physiol 119:1289–1296
Pauw B, Memelink J (2005) Jasmonate-responsive gene expression. J Plant Growth Regul 23:200–210
Pauw B, Hilliou FAO, Martin VS, Chatel G, de Wolf CJF, Champion A, Martial P, 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 279:52940–52948
Peebles CAM, Erik HH, Jacqueline VS, San KY (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 11:76–86
Pieterse CMJ, Antonio LR, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316
Shalel-Levanon S, San KY, Bennett GN (2005) Effect of oxygen, and ArcA and FNR regulators on the expression of genes related to the electron transfer chain and the TCA cycle in Escherichia coli. Metab Eng 7:364–374
Sibéril 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
Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique for RAPD finger print and other PCR applications. Biotechniques 14:748–750
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 1769:139–148
Tikhomiroff C, Jolicoeur M (2002) Screening of Catharanthus roseus secondary metabolites by high-performance liquid chromatography. J Chromatogr A 955:87–93
Van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297
Van der Fits L, Zhang H, Menke FL, Deneka M, Memelink J (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 44:675–685
Weathers PJ, Towler MJ, Xu JF (2010) Bench to batch: advances in plant cell culture for producing useful products. Appl Microbiol Biotechnol 85:1339–1351
Xu MJ, Dong JF (2005) Elicitor-induced nitric oxide burst is essential for triggering catharanthine synthesis in Catharanthus roseus suspension cells. Appl Microbiol Biotechnol 67:40–44
Xu MJ, Dong JF (2007a) Enhancing terpeniod indole alkaloid production by inducible expression of mammalian Bax in Catharanthus roseus cells. Sci China C Life Sci 50:234–241
Xu MJ, Dong JF (2007b) Involvement of nitric oxide signaling in mammalian Bax-induced terpenoid indole alkaloid production of Catharanthus roseus cells. Sci China C Life Sci 50:799–807
Zhang L, Ding RX, Chai YR, Bonfill ME, Oksman-Caldentey KM, Xu TF, Pi Y, Wang ZN, Zhang HM, Kai GY, Liao ZH, Sun XF, Tang KX (2004) Engineering tropane biosynthetic pathway in Hyoscyamus niger hairy root cultures. Proc Natl Acad Sci USA 101:6786–6791
Zhao J, Zhu W, Hu Q (2001) Enhanced catharanthine production in Catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Technol 28:673–681
Zhou ML, Shao JR, Tang YX (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 52:313–323
Acknowledgements
We thank Pang Jun-Feng for technical assistance in RNA extraction and Du Hai for his help in work discussion. We are also grateful to Dr. A.A.N. van Brussel and K. Miettinen (Plant Cell Physiology, Institute of Biology, Leiden University, The Netherlands) for proofreading the manuscript. This work was supported by the National Key Project for Research on Transgenic Biology in China (2008ZX08005-004, 2009ZX08009055B, and 2009ZX08005-004B).
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Zhou, ML., Zhu, XM., Shao, JR. et al. Transcriptional response of the catharanthine biosynthesis pathway to methyl jasmonate/nitric oxide elicitation in Catharanthus roseus hairy root culture. Appl Microbiol Biotechnol 88, 737–750 (2010). https://doi.org/10.1007/s00253-010-2822-x
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DOI: https://doi.org/10.1007/s00253-010-2822-x