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The rolC gene increases caffeoylquinic acid production in transformed artichoke cells

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Abstract

Caffeoylquinic acids are found in artichokes, and they are currently considered important therapeutic or preventive agents for treating Alzheimer’s disease and diabetes. We transformed artichoke [the cultivated cardoon or Cynara cardunculus var. altilis DC (Asteraceae)] with the rolC gene, which is a known inducer of secondary metabolism. High-performance liquid chromatography with UV and high-resolution mass spectrometry (HPLC-UV-HRMS) revealed that the predominant metabolites synthesized in the transgenic calli were 1,5-dicaffeoylquinic acid, 3,4-dicaffeoylquinic acid, and chlorogenic acid. The rolC-transformed calli contained 1.5 % caffeoylquinic acids by dry weight. The overall production of these metabolites was three times higher than that of the corresponding control calli. The enhancing effect of rolC remained stable over long-term cultivation.

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References

  • Bonhomme V, Laurain Mattar D, Fliniaux MA (2000) Effects of the rolC gene on hairy root: induction development and tropane alkaloid production by Atropa belladonna. J Nat Prod 63:1249–1252

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP (2008) Functions of rol genes in plant secondary metabolism. Biotechnol Adv 26:318–324

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Khodakovskaya MV, Labetskaya NV, Chernoded GK, Zhuravlev YN (1998) The impact of plant rolC oncogene on ginsenoside production by ginseng hairy root cultures. Phytochemistry 49:1929–1934

    Article  CAS  Google Scholar 

  • Bulgakov VP, Veselova MV, Tchernoded GK, Kiselev KV, Fedoreyev SA, Zhuravlev YN (2005) Inhibitory effect of the Agrobacterium rhizogenes rolC gene on rabdosiin and rosmarinic acid production in Eritrichium sericeum and Lithospermum erythrorhizon transformed cell cultures. Planta 221:471–478

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Shkryl YN, Veremeichick GN (2010) Engineering high yields of secondary metabolites in Rubia cell cultures through transformation with rol genes. Methods Mol Biol 643:229–242

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Vereshchagina YV (2013) Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotechnol 134:1–22

    PubMed  Google Scholar 

  • Cao X, Xiao H, Zhang Y, Zou L, Chu Y, Chu X (2010) 1,5-Dicaffeoylquinic acid-mediated glutathione synthesis through activation of Nrf2 protects against OGD/reperfusion-induced oxidative stress in astrocytes. Brain Res 1347:142–148

    Article  CAS  PubMed  Google Scholar 

  • Chen R, Liu X, Zou J, Yang L, Dai J (2013) Qualitative and quantitative analysis of phenylpropanoids in cell culture, regenerated plantlets and herbs of Saussurea involucrata. J Pharm Biomed Anal 74:39–46

    Article  CAS  PubMed  Google Scholar 

  • Clément B, Perot J, Geoffroy P, Legrand M, Zon J, Otten L (2007) Abnormal accumulation of sugars and phenolics in tobacco roots expressing the Agrobacterium T-6b oncogene and the role of these compounds in 6b-induced growth. Mol Plant-Microbe Interact 20:53–62

    Article  PubMed  Google Scholar 

  • Clifford MN, Knight S, Kuhnert N (2005) Discriminating between the six isomers of dicaffeoylquinic acid by LC-MS(n). J Agric Food Chem 53:3821–3832

    Article  CAS  PubMed  Google Scholar 

  • Dong GC, Chuang PH, Chang KC, Jan PS, Hwang PI, Wu HB, Yi M, Zhou HX, Chen HM (2009) Blocking effect of an immuno-suppressive agent, cynarin, on CD28 of T-Cell receptor. Pharm Res 26:375–381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gális I, Simek P, Van Onckelen HA, Kakiuchi Y, Wabiko H (2002) Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene, to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol 43:939–950

    Article  PubMed  Google Scholar 

  • Gális I, Kakiuchi Y, Simek P, Wabiko H (2004) Agrobacterium tumefaciens AK-6b gene modulates phenolic compound metabolism in tobacco. Phytochemistry 65:169–179

    Article  PubMed  Google Scholar 

  • Georgiev MI, Eibl R, Zhong JJ (2013) Hosting the plant cells in vitro: recent trends in bioreactors. Appl Microbiol Biotechnol 97:3787–3800

    Article  CAS  PubMed  Google Scholar 

  • Grishchenko OV, Kiselev KV, Tchernoded GK, Fedoreyev SA, Veselova MV, Bulgakov VP, Zhuravlev YN (2013) The influence of the rolC gene on isoflavonoid production in callus cultures of Maackia amurensis. Plant Cell Tissue Organ Cult 113:429–435

    Article  CAS  Google Scholar 

  • Heidarian E, Rafieian-Kopaei M (2013) Protective effect of artichoke (Cynara scolymus) leaf extract against lead toxicity in rat. Pharm Biol 51:1104–1109

    Article  CAS  PubMed  Google Scholar 

  • Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6b oncoproteins. Mol Genet Genomics 267:577–586

    Article  CAS  PubMed  Google Scholar 

  • Inyushkina YV, Kiselev KV, Bulgakov VP, Zhuravlev YN (2009) Specific genes of cytochrome P450 monooxygenases are implicated in biosynthesis of caffeic acid metabolites in rolC-transgenic culture of Eritrichium sericeum. Biochem Mosc 74:917–924

    Article  CAS  Google Scholar 

  • Kakiuchi Y, Gàlis I, Tamogami S, Wabiko H (2006) Reduction of polar auxin transport in tobacco by the tumorigenic Agrobacterium tumefaciens AK-6b gene. Planta 223:237–247

    Article  CAS  PubMed  Google Scholar 

  • Koncz C, Schell J (1986) The promoter of TL-DNA gene 5 controls the tissue-specific expression of chimaeric genes carried by a novel type of Agrobacterium binary vector. Mol Gen Genet 204:383–396

    Article  CAS  Google Scholar 

  • Menin B, Moglia A, Comino C, Lanteri S, Van Herpen TWJM, Beekwilder J (2012) In vitro callogenesis and Agrobacterium-mediated transformation of globe artichoke. 7th International Symposium on In Vitro Culture and Horticultural Breeding. Ghent, Belgium. Book Ser Acta Horticult 961:267–271

    Google Scholar 

  • Miketova P, Schram K, Whitney J, Kearns E, Timmermann B (1999) Mass spectrometry of 3,5- and 4,5-dicaffeoylquinic acids and selected derivatives. J Mass Spectrom 34:1240–1252

    Article  CAS  PubMed  Google Scholar 

  • Moglia A, Lanteri S, Comino C, Acquadro A, de Vos R, Beekwilder J (2008) Stress-induced biosynthesis of dicaffeoylquinic acids in globe artichoke. J Agric Food Chem 56:8641–8649

    Article  CAS  PubMed  Google Scholar 

  • Negro D, Montesano V, Grieco S, Crupi P, Sarli G, De Lisi A, Sonnante G (2012) Polyphenol compounds in artichoke plant tissues and varieties. J Food Sci 77:244–252

    Article  Google Scholar 

  • Nilsson O, Olsson O (1997) Getting to the root: the role of the Agrobacterium rhizogenes rol genes in the formation of hairy roots. Physiol Plant 100:463–473

    Article  CAS  Google Scholar 

  • Palazón J, Cusidó RM, Roig C, Piñol MT (1998a) Expression of the rolC gene and nicotine production in transgenic roots and their regenerated plants. Plant Cell Rep 17:384–390

    Article  Google Scholar 

  • Palazón J, Cusidó RM, Gonzalo J, Bonfill M, Morales S, Piñol MT (1998b) Relation between the amount the rolC gene product and indole alkaloid accumulation in Catharantus roseus transformed root cultures. J Plant Physiol 153:712–718

    Article  Google Scholar 

  • Petersen M, Abdullah Y, Benner J, Eberle D, Gehlen K, Hücherig S, Janiak V, Kim KH, Sander M, Weitzel C, Wolters S (2009) Evolution of rosmarinic acid biosynthesis. Phytochemistry 70:1663–1679

    Article  CAS  PubMed  Google Scholar 

  • Rondanelli M, Giacosa A, Opizzi A, Faliva MA, Sala P, Perna S, Riva A, Morazzoni P, Bombardelli E (2013) Beneficial effects of artichoke leaf extract supplementation on increasing HDL-cholesterol in subjects with primary mild hypercholesterolaemia: a double-blind, randomized, placebo-controlled trial. Int J Food Sci Nutr 64:7–15

    Article  CAS  PubMed  Google Scholar 

  • Rondanelli M, Opizzi A, Faliva M, Sala P, Perna S, Riva A, Morazzoni P, Bombardelli E, Giacosa A (2014) Metabolic management in overweight subjects with naive impaired fasting glycaemia by means of a highly standardized extract from Cynara scolymus: a double-blind, placebo-controlled, randomized clinical trial. Phytother Res 28:33–41

    Article  CAS  PubMed  Google Scholar 

  • Schram K, Miketova P, Slanina J, Humpa O, Taborska E (2004) Mass spectrometry of 1,3- and 1,5-dicaffeoylquinic acids. J Mass Spectrom 39:384–395

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Dai Z, Lu Y (2010) Rapid determination of caffeoylquinic acid derivatives in Cynara scolymus L. by ultrafast liquid chromatography/tandem mass spectrometry based on a fused core C18 column. J Sep Sci 33:3152–3158

    Article  CAS  PubMed  Google Scholar 

  • Shkryl YN, Veremeichik GN, Bulgakov VP, Tchernoded GK, Mischenko NP, Fedoreyev SA, Zhuravlev YN (2008) Individual and combined effects of the rolA, B and C genes on anthraquinone production in Rubia cordifolia transformed calli. Biotechnol Bioeng 100:118–125

    Article  CAS  PubMed  Google Scholar 

  • Slanina J, Táborská E, Bochořákova H, Slaninová I, Humpa O, Robinson WE Jr, Schram KH (2001) New and facile method of preparation of the anti-HIV-1 agent, 1,3-dicaffeoylquinic acid. Tetrahedron Lett 42:3383–3385

    Article  CAS  Google Scholar 

  • Sonnante G, Pignone D, Hammer K (2007) The domestication of artichoke and cardoon: from Roman times to the genomic age. Ann Bot 100:1095–1100

    Article  PubMed Central  PubMed  Google Scholar 

  • Sonnante G, D’Amore R, Blanco E, Pierri CL, De Palma M, Luo J, Tucci M, Martin C (2010) Novel hydroxycinnamoyl-coenzyme A quinate transferase genes from artichoke are involved in the synthesis of chlorogenic acid. Plant Physiol 153:1224–1238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Spena A, Schmülling T, Koncz C, Schell JS (1987) Independent and synergistic activity of rol A, B and C loci in stimulating abnormal growth in plants. EMBO J 6:3891–3899

    CAS  PubMed Central  PubMed  Google Scholar 

  • Takemura T, Urushisaki T, Fukuoka M, Hosokawa-Muto J, Hata T, Okuda Y, Hori S, Tazawa S, Araki Y, Kuwata K (2012) 3,4-Dicaffeoylquinic acid, a major constituent of Brazilian propolis, increases TRAIL expression and extends the lifetimes of mice infected with the influenza A virus. Evid Based Complement Alternat Med. 2012: Article ID 946867, doi: 10.1155/2012/946867

  • Trajtemberg SP, Apóstolo NM, Fernández G (2006) Calluses of Cynara cardunculus var. cardunculus cardoon (Asteraceae): determination of cynarine and chlorogenic acid by automated high-performance capillary electrophoresis. In Vitro Cell Dev Biol Plant 42:534–537

    Article  CAS  Google Scholar 

  • Wang M, Soyano T, Machida S, Yang J-Y, Jung C, Chua N-H, Yuan YA (2011) Molecular insights into plant cell proliferation disturbance by Agrobacterium protein 6b. Genes Dev 25:64–76

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao HB, Cao X, Wang L, Run XQ, Su Y, Tian C, Sun SG, Liang ZH (2011) 1,5-dicaffeoylquinic acid protects primary neurons from amyloid β1-42-induced apoptosis via PI3K/Akt signaling pathway. Chin Med J 124:2628–2635

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the Russian Foundation for Basic Research and the “Molecular and Cell Biology” Grant Program of the Russian Academy of Sciences.

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Authors and Affiliations

  1. Institute of Biology and Soil Science, Far Eastern Branch of the Russian Academy of Sciences, 159 Stoletija Str., Vladivostok, 690022, Russia

    Y. V. Vereshchagina, V. P. Bulgakov, V. P. Grigorchuk, G. N. Veremeichik, G. K. Tchernoded, T. Y. Gorpenchenko, O. G. Koren & Y. N. Zhuravlev

  2. Far Eastern Federal University, Vladivostok, 690950, Russia

    V. P. Bulgakov

  3. A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, 17 Palchevskogo Str., Vladivostok, 690059, Russia

    V. G. Rybin

  4. Tay Nguyen Institute of Scientific Research (TNISR), Vietnam Academy of Science and Technology, 116 Xo Viet Nghe Tinh Street, Dalat City, Vietnam

    N. H. T. Phan, N. T. Minh & L. T. Chau

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  1. Y. V. Vereshchagina
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  2. V. P. Bulgakov
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  3. V. P. Grigorchuk
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  4. V. G. Rybin
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  5. G. N. Veremeichik
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  6. G. K. Tchernoded
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  7. T. Y. Gorpenchenko
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  8. O. G. Koren
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  9. N. H. T. Phan
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  10. N. T. Minh
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  11. L. T. Chau
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  12. Y. N. Zhuravlev
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Corresponding author

Correspondence to V. P. Bulgakov.

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Vereshchagina, Y.V., Bulgakov, V.P., Grigorchuk, V.P. et al. The rolC gene increases caffeoylquinic acid production in transformed artichoke cells. Appl Microbiol Biotechnol 98, 7773–7780 (2014). https://doi.org/10.1007/s00253-014-5869-2

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  • DOI: https://doi.org/10.1007/s00253-014-5869-2

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