Skip to main content
SpringerLink
Log in

Secondary Metabolites in Shoot Cultures of Hypericum

  • Living reference work entry
  • First Online:
Plant Cell and Tissue Differentiation and Secondary Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

  • 142 Accesses

Abstract

The rich phytochemical profile of Hypericum species and the presence of unique compounds, such as hypericins and hyperforin, make them medicinally valuable worldwide. Among Hypericum spp., H. perforatum L. remains the most investigated and exploited species for specific compound production, while others have been surveyed mainly as a source of novel drugs. The main focus of Hypericum biotechnology is the manipulation of secondary metabolism and development of environmentally sustainable and economically viable culture systems toward the efficient production of target and novel secondary metabolites. Since specific compounds accumulate mainly in the aerial parts of Hypericum plants, large-scale shoot cultures are viewed as superior alternative for the production of these compounds under controlled conditions to their extraction from wild- or greenhouse-grown plants or their chemical synthesis. This chapter describes how media culture composition, culture conditions, elicitors, and other critical parameters influence the behavior of Hypericum spp. in shoot cultures and how optimization of these factors could allow improvements in secondary metabolite-related production and discovery of novel drugs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  1. Crockett SL, Robson NKB (2011) Taxonomy and chemotaxonomy of the genus Hypericum. Med Aromat Plant Sci Biotechnol 5(Special Issue 1):1–13

    PubMed  PubMed Central  Google Scholar 

  2. Nürk NM, Crockett SL (2011) Morphological and phytochemical diversity among Hypericum species of the Mediterranean Basin. Med Aromat Plant Sci Biotechnol 5:14–28

    PubMed  PubMed Central  Google Scholar 

  3. Griffith TN, Varela-Nallar L, Dinamarca MC, Inestrosa NC (2010) Neurobiological effects of hyperforin and its potential in Alzheimer’s disease therapy. Curr Med Chem 17(5):391–406. https://doi.org/10.2174/092986710790226156

    Article  CAS  PubMed  Google Scholar 

  4. Güzey G, Sevda I, Öztürk Y, Öztürk N, Maggi F, Sagratini G, Ricciutelli M, Vittori S (2011) Antiproliferative and antioxidant effects of three Hypericum species of Turkish origin: H. perforatum, H. montbretii and H. origanifolium. Med Aromat Plant Sci Biotechnol 5(Special Issue 1):91–99

    Google Scholar 

  5. Borrelli F, Izzo AA (2009) Herb-drug interactions with St John’s wort (Hypericum perforatum): an update on clinical observations. AAPS J 11(4):710–727. https://doi.org/10.1208/s12248-009-9146-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Vattikuti UM, Ciddi V (2005) An overview on Hypericum perforatum Linn. Nat Prod Radiance 4(5):368–381. issn: 0972-592X

    Google Scholar 

  7. Božin B, Kladar N, Grujić N, Anačkov G, Samojlik I, Gavarić N, Conić BS (2013) Impact of origin and biological source on chemical composition anticholinesterase and antioxidant properties of some St. John’s wort species (Hypericum spp. Hypericaceae) from the Central Balkans. Molecules 18:11733–11750. https://doi.org/10.3390/molecules181011733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Karppinen K (2010) Biosynthesis of hypericins and hyperforins in Hypericum perforatum L. (St. John’s wort) – precursors and genes involved. Juvenes Print. ISBN 978-951-42-6309-5. http://jultika.oulu.fi/files/isbn9789514263101.pdf

  9. Patočka J (2003) The chemistry, pharmacology, and toxicology of the biologically active constituents of the herb Hypericum perforatum L. J AppL Biomed 1:61–73. https://doi.org/10.32725/jab.2003.010

    Article  Google Scholar 

  10. Avato P (2005) A survey on the Hypericum genus: secondary metabolites and bioactivity. In: Studies in natural products chemistry-elsevier, vol 30, pp 603–634. https://doi.org/10.1016/S1572-5995(05)80043-2

    Chapter  Google Scholar 

  11. Wilson SA, Roberts SC (2012) Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotechnol J 10:249–268. https://doi.org/10.1111/j.1467-7652.2011.00664.x

    Article  CAS  PubMed  Google Scholar 

  12. Trosset JY, Carbonell P (2015) Synthetic biology for pharmaceutical drug discovery. DrugDes Devel Ther 9:6285. https://doi.org/10.2147/DDDT.S58049

    Article  CAS  Google Scholar 

  13. Murthy HN, Kim YS, Park SY, Paek KY (2014) Hypericins: biotechnological production from cell and organ cultures. Appl Microbiol Biotechnol 98:9187–9198. https://doi.org/10.1007/s00253-014-6119-3

    Article  CAS  PubMed  Google Scholar 

  14. Curtis JD, Lersten NR (1990) Internal secretory structures in Hypericum (Clusiaceae): H. perforatum L. and H. balearicum L. New Phytol 114:571–580

    Article  Google Scholar 

  15. Fornasiero RB, Bianchi A, Pinetti A (1998) Anatomical and ultrastructural observations in Hypericum perforatum L. leaves. J Herbs Spices Med Plants 5:21–33. https://doi.org/10.1300/J044v05n04_04

    Article  Google Scholar 

  16. Zobayed SMA, Afreen F, Goto E, Kozai T (2006) Plant–environment interactions: accumulation of hypericin in dark glands of Hypericum perforatum. Ann Bot 98:793–804. https://doi.org/10.1093/aob/mcl169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Soelberg J, Jørgensen LB, Jäger AK (2007) Hyperforin accumulates in the translucent glands of Hypericum perforatum. Ann Bot 99:1097–1100. https://doi.org/10.1093/aob/mcm057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kirakosyan A, Gibson DM, Kaufman PB (2008) The production of dianthrones and phloroglucinol derivatives in St. John’s wort. In: Ramawat KG, Mérillon JM (eds) Bioactive molecules and medicinal plants. Springer, pp 149–164. https://doi.org/10.1007/978-3-540-74603-4_7

    Chapter  Google Scholar 

  19. Kirakosyan A, Gibson DM, Sirvent TM (2003) A comparative study of Hypericum perforatum plants as sources of hypericins and hyperforins. J Herbs Spices Med Plants 10:73–88. https://doi.org/10.1300/J044v10n04_08

    Article  CAS  Google Scholar 

  20. Varghese RJ, Sooriamuthu S (2013) Differences in hypericin synthesis between experimentally induced seedling shoot cultures of Hypericum hookerianum Wight & Arn. Plant Biotechnol Rep 7:511–518. https://doi.org/10.1007/s11816-013-0289-9

    Article  Google Scholar 

  21. Karioti A, Bilia AR (2010) Hypericins as potential leads for new therapeutics. Int J Mol Sci 11:562–594. https://doi.org/10.3390/ijms11020562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jakubowska M, Michalczyk W, Pyka DJ, Susz A, Urbanska K, Płonka BK, Kuleta P, Łącki P, Krzykawska-Serda M, Fiedor L, Płonka PM (2013) Nitrosylhemoglobin in photodynamically stressed human tumors growing in nude mice. Nitric Oxide 35:79–88. https://doi.org/10.1016/j.niox.2013.08.004

    Article  CAS  PubMed  Google Scholar 

  23. Velingkar VS, Gupta GL, Hegde NB (2017) A current update on phytochemistry, pharmacology and herb–drug interactions of Hypericum perforatum. Phytochem Rev 16(4):725–744. https://doi.org/10.1007/s11101-017-9503-7

    Article  CAS  Google Scholar 

  24. Kimáková K, Petijová L, Bruňáková K, Čellarová E (2018) Relation between hypericin content and morphometric leaf parameters in Hypericum spp.: a case of cubic degree polynomial function. Plant Sci 271:94–99. https://doi.org/10.1016/j.plantsci.2018.03.019

    Article  CAS  PubMed  Google Scholar 

  25. Agapouda A, Bookera A, Kiss T, Hohmann J, Heinrich M, Csupor D (2017) Quality control of Hypericum perforatum L. analytical challenges and recent progress. J Pharm Pharmacol 71:15–37. https://doi.org/10.1111/jphp.12711

    Article  CAS  PubMed  Google Scholar 

  26. EMEA (2009) European medicines agency evaluation of medicines for human use. Committee on herbal medicinal products (HMPC) assessment report on Hypericum perforatum L, herba. London, Doc. Ref.: EMA/HMPC/101303/2008

    Google Scholar 

  27. Galeotti N (2017) Hypericum perforatum (St John’s wort) beyond depression: a therapeutic perspective for pain conditions. J Ethnopharmacol 200:136–146. https://doi.org/10.1016/j.jep.2017.02.016

    Article  CAS  PubMed  Google Scholar 

  28. Ivanova D, Gerova D, Chervenkov T, Yankova T (2005) Polyphenols and antioxidant capacity of Bulgarian medicinal plants. J Ethnopharmacol 96(1–2):145–150. https://doi.org/10.1016/j.jep.2004.08.033

    Article  CAS  PubMed  Google Scholar 

  29. Kultur S (2007) Medicinal plants used in Kırklareli Province (Turkey). J Ethnopharmacol 111(2):341–364. https://doi.org/10.1016/j.jep.2006.11.035

    Article  PubMed  Google Scholar 

  30. Kitanov GM (2001) Hypericin and pseudohypericin in some Hypericum species. Biochem Syst Ecol 29(2):171–178. https://doi.org/10.1016/S0305-1978(00)00032-6

    Article  CAS  PubMed  Google Scholar 

  31. Liu X-N, Zhang X-Q, Sun J-S (2007) Effects of cytokinins and elicitors on the production of hypericins and hyperforin metabolites in Hypericum sampsonii and Hypericum perforatum. Plant Growth Regul 53:207–214. https://doi.org/10.1007/s10725-007-9220-0

    Article  CAS  Google Scholar 

  32. Ayan AK, Çirak C (2008) Hypericin and pseudohypericin contents in some Hypericum species growing in Turkey. Pharm Biol 46:288–291. https://doi.org/10.1080/13880200701741211

    Article  CAS  Google Scholar 

  33. Kusari S, Zühlke S, Borsch T, Spiteller M (2009) Positive correlations between hypericin and putative precursors detected in the quantitative secondary metabolite spectrum of Hypericum. Phytochemistry 70(10):1222–1232. https://doi.org/10.1016/j.phytochem.2009.07.022

    Article  CAS  PubMed  Google Scholar 

  34. Ҫirak C, Radusiene J, Arslan B (2008) Variation of bioactive substances in Hypericum montbretii during plant growth. Nat Prod Res 22(3):246–252. https://doi.org/10.1080/14786410701642623

    Article  CAS  Google Scholar 

  35. Bagdonaitė E, Janulis V, Ivanauskas L, Labokas J (2012) Between species diversity of Hypericum perforatum and H. maculatum by the content of bioactive compounds. Nat Prod Commun 7(2):199–200

    PubMed  Google Scholar 

  36. Mártonfi P, Repčák M, Zanvit P (2006) Secondary metabolites variation in Hypericum maculatum and its relatives. Biochem Syst Ecol 34(1):56–59. https://doi.org/10.1016/j.bse.2005.07.008

    Article  CAS  Google Scholar 

  37. Gudžić BT, Smelcerovic A, Dordevic S, Mimica-Dukic N, Ristic M (2007) Essential oil composition of Hypericum hirsutum L. Flavour Fragr J 22:42–43. https://doi.org/10.1002/ffj.1749

    Article  CAS  Google Scholar 

  38. Oniga I, Toiu A, Benedec D, Tomuta I, Vlase L (2016) Phytochemical analysis of Hypericum maculatum in order to obtain standardized extracts. Farmacia 64(2):171–174

    CAS  Google Scholar 

  39. Stojanović G, Ðorđević A, Šmelcerović A (2013) Do other Hypericum species have medical potential as St. John’s wort (Hypericum perforatum)? Curr Med Chem 20:2273–2295. https://doi.org/10.2174/0929867311320180001

    Article  PubMed  Google Scholar 

  40. Mir MY, Hamid S, Kamili AN, Hassan OP (2019) Sneak peek of Hypericum perforatum L.: phytochemistry, phytochemical efficacy and biotechnological interventions. J Plant Biochem Biotech. https://doi.org/10.1007/s13562-019-00490-7

    Article  CAS  Google Scholar 

  41. Crockett SL, Kunert O, Pferschy-Wenzig E-M, Jacob M, Schuehly W, Bauer R (2016) Phloroglucinol and Terpenoid derivatives from Hypericum cistifolium and H. galioides (Hypericaceae). Front Plant Sci. https://doi.org/10.3389/fpls.2016.00961

  42. Guedes AP, Franklin G, Fernandes-Ferreira M (2012) Hypericum spp.: essential oil composition and biological activities. Phytochem Rev 11:127–152. https://doi.org/10.1007/s11101-012-9223-y

    Article  CAS  Google Scholar 

  43. Bruni R, Sacchetti G (2009) Factors affecting polyphenol biosynthesis in wild and field grown St. John’s wort (Hypericum perforatum L. Hypericaceae/Guttiferae). Molecules 14(2):682–725. https://doi.org/10.3390/molecules14020682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cseke LJ, Kirakosyan A, Kaufman PB, Warber SL, Duke JA, Brielmann HI (2006) Natural product from plants. CRC Press Taylor & Francis Group, LLC United States of America. ISBN 0-8493-2976-0

    Google Scholar 

  45. Franklin G, Beerhues L, Čellárová E (2017) Molecular and biotechnological advancements in Hypericum species. Front Plant Sci 7:1687. https://doi.org/10.3389/fpls.2016.01687

    Article  Google Scholar 

  46. Cui XH, Murthy HN, Wu CH, Paek KY (2010) Adventitious root suspension cultures of Hypericum perforatum: effect of nitrogen source on production of biomass and secondary metabolites. In Vitro Cell Dev Biol-Plant 46(5):437–444. https://doi.org/10.1007/s11627-010-9310-y

    Article  CAS  Google Scholar 

  47. Wu SQ, Yu XK, Lian ML, Park SY, Piao XC (2014) Several factors affecting hypericin production of Hypericum perforatum during adventitious root culture in airlift bioreactors. Physiol Plant 36(4):975–981. https://doi.org/10.1007/s11738-013-1476-6

    Article  CAS  Google Scholar 

  48. Čellárová E (2003) Culture and biotechnology of Hypericum. In: Ernst E (ed) Hypericum: the genus Hypericum, medicinal and aromatic plants-industrial profiles, vol 31. CRC Press/Taylor & Francis, London/New York, pp 65–76

    Google Scholar 

  49. Kirakosyan A (2006) Plant biotechnology for the production of natural products. In: Brielmann HL, Kaufman PB, Duke JA, Cseke LJ, Warber SL, Kirakosyan A (eds) Natural products from plants, 2nd edn. CRC Press/Taylor & Francis, Boca Raton, pp 221–262

    Chapter  Google Scholar 

  50. Kartnig T, Göbel I, Heydel B (1996) Production of hypericin, pseudohypericin and flavonoids in cell cultures of various Hypericum species and their chemotypes. Planta Med 62:51–53. https://doi.org/10.1055/s-2006-957796

    Article  CAS  PubMed  Google Scholar 

  51. Mederos-Molina S (2002) Micropropagation of Hypericum canariense for the production of hypericin. In: Nagata T, Ebizuka Y (eds) Biotechnology in agriculture and forestry, Medicinal and Aromatic Plants XII, vol 51. Springer, Berlin/Heidelberg, pp 95–117

    Google Scholar 

  52. Karakas O, Toker Z, Tilkat E, Ozen HC, Onay A (2009) Effects of different concentrations of benzylaminopurine on shoot regeneration and hypericin content in Hypericum triquetrifolium Turra. Nat Prod Res 23(16):1459–1465. https://doi.org/10.1080/14786410701664528

    Article  CAS  PubMed  Google Scholar 

  53. Coste A, Vlase L, Halmagyi A, Deliu C, Coldea G (2011) Effects of plant growth regulators and elicitors on production of secondary metabolites in shoot cultures of Hypericum hirsutum and Hypericum maculatum. Plant Cell Tissue Organ Cult 106:279–288. https://doi.org/10.1007/s11240-011-9919-5

    Article  CAS  Google Scholar 

  54. Danova K, Nikolova-Damianova B, Denev R, Dimitrov D (2012) Influence of vitamins on polyphenolic content, morphological development, and stress response in shoot cultures of Hypericum spp. Plant Cell Tiss Organ Cult 110:383–393. https://doi.org/10.1007/s11240-012-0159-0

    Article  CAS  Google Scholar 

  55. Rainha N, Lima E, Batista J, Fernandes-Ferreira M (2012) Content of hypericins from plants and in vitro shoots of Hypericum undulatum Schousb. ex Willd. Nat Prod Res 27:869–879. https://doi.org/10.1080/14786419.2012.688051

    Article  CAS  PubMed  Google Scholar 

  56. Gadzovska S, Maury S, Ounnar S, Righezza M, Kascakova S, Refregiers M, Spasenoski M, Joseph C, Hagège D (2005) Identification and quantification of hypericin and pseudohypericin in different Hypericum perforatum L. in vitro cultures. Plant Physiol Biochem 43:591–601. https://doi.org/10.1016/j.plaphy.2005.05.005

    Article  CAS  PubMed  Google Scholar 

  57. Gadzovska S, Maury S, Delaunay A, Spasenoski M, Joseph C, Hagège D (2007) Jasmonic acid elicitation of Hypericum perforatum L. cell suspensions and effects on the production of phenylpropanoids and naphtodianthrones. Plant Cell Tissue Organ Cult 89(1):1–13. https://doi.org/10.1007/s11240-007-9203-x

    Article  CAS  Google Scholar 

  58. Gadzovska Simic S, Tusevski O, Antevski S, Atanasova-Pancevska N, Petreska J, Stefova M, Kungulovski D, Spasenoski M (2012) Secondary metabolite production in Hypericum perforatum L. cell suspensions upon elicitation with fungal mycelia from Aspergillus flavus. Arch Biol Sci 64:113–121. https://doi.org/10.2298/ABS1201113G

    Article  Google Scholar 

  59. Gadzovska S, Maury S, Delaunay A, Spasenoski M, Hagège D, Courtois D, Joseph C (2013) The influence of salicylic acid elicitation of shoots, callus and cell suspension cultures on production of naphtodianthrones and phenylpropanoids in Hypericum perforatum L. Plant Cell Tiss Org Cult 113:25–39. https://doi.org/10.1007/s11240-012-0248-0

    Article  CAS  Google Scholar 

  60. Liu XN, Zhang XQ, Zhang SX, Sun JS (2007) Regulation of metabolite production by precursors and elicitors in liquid cultures of Hypericum perforatum. Plant Cell Tiss Organ Cult 91:1–7. https://doi.org/10.1007/s11240-007-9271-y

    Article  CAS  Google Scholar 

  61. Tusevski O, Stanoeva JP, Stefova M, Gadzovska-Simic S (2015) Agrobacterium enhances xanthone production in Hypericum perforatum cell suspensions. Plant Growth Regul 76(2):199–210. https://doi.org/10.1007/s10725-014-9989-6

    Article  CAS  Google Scholar 

  62. Hou W, Preeti S, Franklin G (2016) A Perspective on Hypericum perforatum Genetic Transformation. Front Plant Sci 7:879. https://doi.org/10.3389/fpls.2016.00879

    Article  PubMed  PubMed Central  Google Scholar 

  63. Santarem ER, Zamban DC, Astarita LV (2003) Multiple shoot formation in Hypericum perforatum L and hypericin production. In Vitro Cell Dev Biol Anim 44:S52. http://www.scielo.br/pdf/bjpp/v15n1/a06v15n1.pdf

    Google Scholar 

  64. Danova K (2010) Production of polyphenolic compounds in shoot cultures of Hypericum species characteristic for the Balkan flora. Botanica Serbica 34:29–36

    Google Scholar 

  65. Karppinen K, Hokkanen J, Tolonen A, Mattila S, Hohtola A (2007) Biosynthesis of hyperforin and adhyperforin from amino acid precursors in shoot cultures of Hypericum perforatum. Phytochemistry 68:1038–1045. https://doi.org/10.1016/j.phytochem.2007.01.001

    Article  CAS  PubMed  Google Scholar 

  66. Sood H, Shitiz K, Sharma N (2015) Rapid method for in vitro multiplication of hypericin rich shoots of Hypericum perforatum. J Plant Sci 3:279–284. https://doi.org/10.11648/j.jps.20150305.16

    Article  Google Scholar 

  67. Asan HS, Ozen HC, Onay A, Asan N (2015) Effect of BAP on total hypericin production in shoot cultures of Hypericum scabroides: an endemic species in the eastern Anatolia region of Turkey. Eurasia J Biosci 9:46–51. https://doi.org/10.5053/ejobios.2015.9.0.6

    Article  CAS  Google Scholar 

  68. Yazaki K, Okuda T (1990) Procyanidins in callus and multiple shoot cultures of Hypericum erectum. Planta Med 56:490–491. https://doi.org/10.1055/s-2006-961020

    Article  CAS  PubMed  Google Scholar 

  69. Figueiró AA, Correa CM, Astarita LV, Santarém ER (2010) Long-term maintenance of in vitro cultures affects growth and secondary metabolism of St. John’s wort. Ciência Rural Santa Maria 40(10):2115–2121. https://doi.org/10.1590/S0103-84782010001000010

    Article  Google Scholar 

  70. Kornfeld A, Kaufman PB, Lu CR, Gibson DM, Bolling SF, Warber SL, Chang SC, Kirakosyan A (2007) The production of hypericins in two selected Hypericum perforatum shoot cultures is related to differences in black gland structure. Plant Physiol Biochem 45:24–32. https://doi.org/10.1016/j.plaphy.2006.12.009

    Article  CAS  PubMed  Google Scholar 

  71. Mulinacci N, Giaccherini C, Santamaria AR, Caniato R, Ferrari F, Valleta A, Vincieri FF, Pasqua G (2008) Anthocyanins and xanthones in the calli and shoots of Hypericum perforatum var. angustifolium (sin. Fröhlich) Bork.. Plant Physiol Biochem 46:414–420. https://doi.org/10.1016/j.plaphy.2007.12.005

    Article  CAS  PubMed  Google Scholar 

  72. Bernardi APM, Maurmann N, Rech SB, von Poser G (2007) Benzopyrans in Hypericum polyanthemum Klotzsch ex Reichardt cultured in vitro. Acta Physiol Plant 29:165–170. https://doi.org/10.1007/s11738-006-0021-2

    Article  CAS  Google Scholar 

  73. Khlifa HD, Ibrahim IA, Bekhit M, Szkop M, Taha HS (2016) Hypericum sinaicum L. in vitro regeneration and analysis of hypericin content. Intl J Curr Microbiol App Sci 5:182–196. https://doi.org/10.20546/ijcmas.2016.508.020

    Article  CAS  Google Scholar 

  74. Shilpashree HP, Ravishankar Rai V (2009) In vitro plant regeneration and accumulation of flavonoids in Hypericum mysorense. Intl J Integr Biol 8:43–49

    CAS  Google Scholar 

  75. Pavlik M, Vacek J, Klejdus B (2007) Hypericin and hyperforin production in St. John’s wort in vitro culture: influence of saccharose, polyethylene glycol, methyl jasmonate and Agrobacterium tumefaciens. J Agric Food Chem 55:6147–6153. https://doi.org/10.1021/jf070245w

    Article  CAS  PubMed  Google Scholar 

  76. Kirakosyan A, Hayashi H, Inoue K, Charchoglyan A, Vardapetyan H (2000) Stimulation of the production of hypericins by mannan in Hypericum perforatum shoot cultures. Phytochemistry 53(3):345–348. https://doi.org/10.1016/S0031-9422(99)00496-3

    Article  CAS  PubMed  Google Scholar 

  77. Gadzovska-Simic S, Tusevski O, Maury S, Delaunay A, Joseph C, Hagège D (2014) Effects of polysaccharide elicitors on secondary metabolite production and antioxidant response in Hypericum perforatum L shoot cultures. Sci World J:609649. https://doi.org/10.1155/2014/609649

    Article  Google Scholar 

  78. Sooriamuthu S, Varghese RJ, Bayyapureddy A, John SST, Narayanan R (2013) Light-induced production of antidepressant compounds in etiolated shoot cultures of Hypericum hookerianum Wight & Arn. (Hypericaceae). Plant Cell Tissue Organ Cult 115(2):169–178. https://doi.org/10.1007/s11240-013-0350-y

    Article  CAS  Google Scholar 

  79. Zobayed SMA, Murch SJ, Rupasinghe HPV, Saxena PK (2003) Elevated carbon supply altered hypericin and hyperforin contents of St. John’s wort (Hypericum perforatum) grown in bioreactors. Plant Cell Tissue Organ Cult 75(2):143–149. https://doi.org/10.1023/A:1025053427371

    Article  CAS  Google Scholar 

  80. Yamaner O, Erdag B (2013) Effects of sucrose and polyethylene glycol on hypericins content in Hypericum adenotrichum. EurAsian J Biosci 7(1):101–110. https://doi.org/10.5053/ejobios.2013.7.0.12

    Article  CAS  Google Scholar 

  81. Tusevski O, Petreska Stanoeva J, Stefova M, Pavokovic D, Gadzovska Simic S (2014) Identification and quantification of phenolic compounds in Hypericum perforatum L. transgenic shoots. Acta Physiol Plant 36(10):2555–2569. https://doi.org/10.1007/s11738-014-1627-4

    Article  CAS  Google Scholar 

  82. Nigutová K, Kusari S, Sezgin S, Petijová L, Henzelyová J, Bálintová M, Spiteller M, Čellárová E (2017) Chemometric evaluation of hypericin and related phytochemicals in 17 in vitro cultured Hypericum species, hairy root cultures and hairy root derived transgenic plants. J Pharm Pharmacol. https://doi.org/10.1111/jphp.12782

    Article  PubMed  Google Scholar 

  83. Khan SA, Verma P, Arbat A, Gaikwad S, Parasharami VA (2018) Development of enhanced hypericin yielding transgenic plants and somaclones: high throughout direct organogenesis from leaf and callus explants of Hypericum perforatum. Ind Crops Prod 111:544–554. https://doi.org/10.1016/j.indcrop.2017.11.032

    Article  CAS  Google Scholar 

  84. Kwiecień I, Smolin J, Beerhues L, Ekiert H (2018) The impact of media composition on production of flavonoids in agitated shoot cultures of the three Hypericum perforatum L. In Vitro Cell Dev Biol Plant 54:332–340. https://doi.org/10.1007/s11627-018-9900-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Savio LEB, Astarita LV, Santarém ER (2012) Secondary metabolism in micropropagated Hypericum perforatum L. grown in nonaerated liquid medium. Plant Cell Tiss Organ Cult 108:465–472. https://doi.org/10.1007/s11240-011-0058-9

    Article  CAS  Google Scholar 

  86. Murch SJ, Saxena PK (2006) A melatonin-rich germplasm line of St John’s wort (Hypericum perforatum L.). J Pineal Res 41(3):284–287. https://doi.org/10.1111/j.1600-079X.2006.00367.x

    Article  CAS  PubMed  Google Scholar 

  87. Danova K, Čellárová E, Macková A, Daxnerová Z, Kapchina-Toteva V (2010) In vitro culture of Hypericum rumeliacum Boiss. And production of phenolics and flavonoids. In Vitro Cell Dev Biol-Plant 46:422–429. https://doi.org/10.1007/s11627-010-9299-2

    Article  CAS  Google Scholar 

  88. Jamwal K, Bhattacharya S, Puri S (2018) Plant growth regulator mediated consequences of secondary metabolites in medicinal plants. J App Res Med Arom Plants 9:26–38. https://doi.org/10.1016/j.jarmap.2017.12.003

    Article  Google Scholar 

  89. Shakya P, Marslin G, Siram K, Beerhues L, Franklin G (2019) Elicitation as a tool to improve the profiles of high-value secondary metabolites and pharmacological properties of Hypericum perforatum. J Pharm Pharmacol 71(1):70–82. https://doi.org/10.1111/jphp.12743

    Article  CAS  PubMed  Google Scholar 

  90. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

    Article  CAS  Google Scholar 

  91. Čellárová E (2011) Effect of exogenous morphogenetic signals on differentiation in vitro and secondary metabolite formation in the genus Hypericum. In: Odabs MS, Çirak C (eds) Medicinal and aromatic plant science and biotechnology, vol 5. Global Science Books, pp 62–69. http://www.globalsciencebooks.info/Online/GSBOnline/images/2011/MAPSB_5(SI1)/MAPSB_5(SI1)62-69o.pdf

  92. Dias ACP, Seabra RM, Andrade PB, Ferreira MF (1999) The development and evaluation of a HPLC–DAD method for the analysis of the phenolic fractions from in vivo and in vitro biomass of Hypericum species. J Liq Chromatogr 22:215–227. https://doi.org/10.1081/JLC-100101655

    Article  CAS  Google Scholar 

  93. Pasqua G, Avato P, Monacelli B, Santamaria AR, Argentieri MP (2003) Metabolites in cell suspension cultures, calli, and in vitro regenerated organs of Hypericum perforatum cv. Topas. Plant Sci 165(5):977–982. https://doi.org/10.1016/S0168-9452(03)00275-9

    Article  CAS  Google Scholar 

  94. Bertoli A, Giovannini A, Ruffoni B, Guardo AD, Spinelli G, Mazzetti M, Pistelli L (2008) Bioactive constituent production in St. John’s wort in vitro hairy roots. Regenerated plant lines. J Agric Food Chem 56(13):5078–5082. https://doi.org/10.1021/jf0729107

    Article  CAS  PubMed  Google Scholar 

  95. Čellárová E, Kimáková K, Daxnerová Z, Mártonfi P (1995) Hypericum perforatum (St. John’s wort): in vitro culture and the production of hypericin and other secondary metabolites. In: YPS B (ed) Medicinal and aromatic plants VIII. Springer, Berlin, pp 262–272

    Google Scholar 

  96. Rani NS, Balaji K, Ciddi V (2001) Production of hypericin from tissue culture of Hypericum perforatum. Indian J Pharm Sci 63:432–433

    Google Scholar 

  97. Muszyńska B, Ekiert H, Kwiecień I, Maślanka A, Zodi R, Beerhues L (2014) Comparative analysis of therapeutically important indole compounds in in vitro cultures of Hypericum perforatum cultivars by HPLC and TLC analysis coupled with densitometric detection. Nat Prod Commun 9(10):1437–1440

    PubMed  Google Scholar 

  98. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50(1):151–158. https://doi.org/10.1016/0014-4827(68)90403-5

    Article  CAS  PubMed  Google Scholar 

  99. Treneva G, Markovska Y, Wolfram E, Danova K (2014) Effect of plant growth regulators on growth patterns and enzymatic antioxidant activities in Hypericum calycinum shoot cultures. Bulgarian J Agr Sci 20:46–50. https://doi.org/10.21256/zhaw-4132

    Article  Google Scholar 

  100. Guedes AP, Amorim LR, Vicente AM, Ramos G, Fernandes-Ferreira M (2003) Essential oils from plants and in vitro shoots of Hypericum androsaemum L. J Agric Food Chem 51(5):1399–1404

    Article  CAS  PubMed  Google Scholar 

  101. Margara J (1984) Bases de la Multiplication Vegetative. INRA, Versalles/Paris

    Google Scholar 

  102. Guedes AP (2009) Essential oils from plants and in vitro shoot cultures of Hypericum androsaemum L., H. perforatum L. and H. undulatum Schousboe ex. Wild. Ph.D. thesis, Universidade do Minho. http://hdl.handle.net/1822/9876

  103. Park S, Ahn IS, Kim JH, Lee MR, Kim JS, Kim HJ (2010) Glyceollins one of the phytoalexins derived from soybeans under fungal stress enhance insulin sensitivity and exert insulinotropic actions. J Agric Food Chem 58:1551–1557. https://doi.org/10.1021/jf903432b

    Article  CAS  PubMed  Google Scholar 

  104. Ramakrishna A, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6(11):1720–1731. https://doi.org/10.4161/psb.6.11.17613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Yamaner Ö, Erdag B, Cengiz G (2013) Stimulation of the production of hypericins in in vitro seedlings of Hypericum adenotrichum by some biotic elicitors. Turk J Bot 37:153–159. https://doi.org/10.3906/bot-1202-1

    Article  CAS  Google Scholar 

  106. Meirelles G, Valle Pinhatti A, Sosa-Gomez D, Gonçalves Rosa LMR, von Poser GL (2013) Influence of fungal elicitation with Nomuraea rileyi (Farlow) Samson in the metabolism of acclimatized plants of Hypericum polyanthemum Klotzsech ex Reichardt (Guttiferae). Plant Cell Tiss Organ Cult 112(3):379–385. https://doi.org/10.1007/s11240-012-0234-6

    Article  CAS  Google Scholar 

  107. Bálintová M, Bruňáková K, Petijová L, Čellárová E (2019) Targeted metabolomic profiling reveals interspecific variation in the genus Hypericum in response to biotic elicitors. Plant Physiol Biochem 135:348–358. https://doi.org/10.1016/j.plaphy.2018.12.024

    Article  CAS  PubMed  Google Scholar 

  108. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507. https://doi.org/10.1105/tpc.104.026765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428(6984):764–767. https://doi.org/10.1038/nature02485

    Article  CAS  PubMed  Google Scholar 

  110. Santarem ER, Zamban DC, Felix LM, Astarita LV (2008) Secondary metabolism of Hypericum perforatum induced by Agrobacterium rhizogenes. In Vitro Cell Dev Biol Anim 44:S52

    Article  Google Scholar 

  111. Santarem E, Silva T, Freitas K, Sartor T, Astarita L (2010) Agrobacterium rhizogenes and salicylic acid trigger defense responses in Hypericum perforatum shoots. In Vitro Cell Dev Biol Anim 46:S159–S160

    Google Scholar 

  112. Mañero FJG, Algar E, Martín Gómez MS, Saco Sierra MD, Solano BR (2012) Elicitation of secondary metabolism in Hypericum perforatum by rhizosphere bacteria and derived elicitors in seedlings and shoot cultures. Pharm Biol 50(10):1201–1209. https://doi.org/10.3109/13880209.2012.664150

    Article  CAS  PubMed  Google Scholar 

  113. Azeez H, Ibrahim K (2013) Effect of biotic elicitors on secondary metabolite production in cell suspensions of Hypericum triquetrifolium Turra. Bull Univ Agric Sci Vet Med Cluj-Napoca Horticul 70:26–33. https://doi.org/10.15835/buasvmcn-hort:9264

    Article  Google Scholar 

  114. Franklin G, Dias A (2011) Hypericum perforatum cells accumulate anthocyanins and flavonoids at the expense of xanthone biosynthesis during light adaptation Plant Engine. http://www.plantengine.eu/sites/default/files/Book%20of%20Abstracts%20Murcia%202011_0.pdf

  115. Zhao J, Liua W, Wang J-C (2015) Recent advances regarding constituents and bioactivities of plants from the genus Hypericum. Chem Biodivers 12:309–349. https://doi.org/10.1002/cbdv.201300304

    Article  CAS  PubMed  Google Scholar 

  116. Zobayed S, Saxena PK (2004) Production of St. john’s wort plants under controlled environment for maximizing biomass and secondary metabolites. In Vitro Cell Dev Biol Plant 40:108–114. https://doi.org/10.1079/IVP2003498

    Article  CAS  Google Scholar 

  117. Bruňáková K, Čellárová E (2017) Modulation of anthraquinones and phloroglucinols biosynthesis in Hypericum spp. by cryogenic treatment. Biotechnol 251:59–67. https://doi.org/10.1016/j.jbiotec.2017.04.012

    Article  CAS  Google Scholar 

  118. Tirillini B, Ricci A, Pintore G, Chessa M, Sighinolfi S (2006) Induction of hypericins in Hypericum perforatum in response to chromium. Fitoterapia 77(3):164–170. https://doi.org/10.1016/j.fitote.2006.01.011

    Article  CAS  PubMed  Google Scholar 

  119. Murch SJ, Haq K, Vasantha Rupashige HP, Saxena PK (2003) Nickel contamination affects growth and secondary metabolite composition of St. John’s wort (Hypericum perforatum L.). Environ Exp Bot 49:251–257. https://doi.org/10.1016/S0098-8472(02)00090-4

    Article  CAS  Google Scholar 

  120. Yamaner Ö, Erdağ B (2018) Chrome elicitation for secondary metabolites stimulation in Hypericum adenotrichum Spach. Eur J Biotechnol Biosci 6(5):52–55

    Google Scholar 

  121. Zhang B, Zheng LP, Li WY, Wang JW (2013) Stimulation of artemisinin production in Artemisia annua hairy roots by Ag-SiO2 core-shell nanoparticles. Curr Nanosci 9(3):363–370. https://doi.org/10.2174/1573413711309030012

    Article  CAS  Google Scholar 

  122. Ghanati F, Bakhtiarian S (2014) Effect of methyl jasmonate and silver nanoparticles on production of secondary metabolites by Calendula officinalis L (Asteraceae). Trop J Pharm Res 13:1783–1789. https://doi.org/10.4314/tjpr.v13i11.2

    Article  CAS  Google Scholar 

  123. Ghorbanpour M, Hadian J (2015) Multiwalled carbon nanotubes stimulate callus induction secondary metabolites biosynthesis and antioxidant capacity in medicinal plant Satureja khuzestanica grown in vitro. Carbon 94:749–759. https://doi.org/10.1016/j.carbon.2015.07.056

    Article  CAS  Google Scholar 

  124. Sharafi E, Nekoei SMK, Fotokian MH, Davoodi D, Mirzaei HH, Hasanloo T (2013) Improvement of hypericin and hyperforin production using zinc and iron nano-oxides as elicitors in cell suspension culture of St John’s wort (Hypericum perforatum L.). J Med Plants By-Prod 2:177–184

    Google Scholar 

  125. Schlipf DM, Jones CA, Armbruster ME, Rushing ES, Wooten KC, Rankin SE, Knutson BL (2015) Flavonoid adsorption and stability on titania functionalized silica nanoparticles. Colloids Surf A 478:15–21. https://doi.org/10.1016/j.colsurfa.2015.03.039

    Article  CAS  Google Scholar 

  126. Uma RM, Gaviraj EN, Veeresham C (2011) Enhanced production of Hypericins in shoot cultures of Hypericum Perforatum by interference with precursor metabolism. Int J Pharm Bio Sci 7(14). issn: NO-2230-7885

    Google Scholar 

  127. Di Guardo A, Čellarová E, Koperdáková J, Pistelli L, Ruffoni B, Allavena A, Giovannini A (2003) Hairy roots induction and plant regeneration in Hypericum perforatum L. J Genet Breed 57:269–278

    Google Scholar 

  128. Franklin G, Oliveira M, Dias ACP (2007) Production of transgenic Hypericum perforatum plants via particle bombardment-mediated transformation of novel organogenic cell suspension cultures. Plant Sci 172:1193–1203. https://doi.org/10.1016/j.plantsci.2007.02.017

    Article  CAS  Google Scholar 

  129. Komarovská H, Giovannini A, Košuth J, Čellárová E (2009) Agrobacterium rhizogenes-mediated transformation of Hypericum tomentosum L. and Hypericum tetrapterum fries. Z Naturforsch 64(11–12):864–868

    Article  Google Scholar 

  130. Kumar N, Gulati A, Bhattacharya A (2013) L-glutamine and L-glutamic acid facilitate successful Agrobacterium infection of recalcitrant tea cultivars. Appl Biochem Biotechnol 170(7):1649–1664. https://doi.org/10.1007/s12010-013-0286-z

    Article  CAS  PubMed  Google Scholar 

  131. Dan Y (2008) Biological functions of antioxidants in plant transformation. In Vitro Cell Dev Biol Plant 44(3):149–161. https://doi.org/10.1007/s11627-008-9110-9

    Article  CAS  Google Scholar 

  132. Dan Y, Baxter A, Zhang S, Pantazis CJ, Veilleux RE (2010) Development of efficient plant regeneration and transformation system for impatiens using Agrobacterium tumefaciens and multiple bud cultures as explants. BMC Plant Biol 10:165. https://doi.org/10.1186/1471-2229-10-165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Dan Y, Zhang S, Zhong H, Yi H, Sainz MB (2015) Novel compounds that enhance Agrobacterium-mediated plant transformation by mitigating oxidative stress. Plant Cell Rep 34:291–309. https://doi.org/10.1007/s00299-014-1707-3

    Article  CAS  PubMed  Google Scholar 

  134. Wang YP, Sonntag K, Rudloff E, Han J (2005) Production of fertile transgenic Brassica napus by Agrobacterium-mediated transformation of protoplasts. Plant Breed 124:1–4. https://doi.org/10.1111/j.1439-0523.2004.01015.x

    Article  CAS  Google Scholar 

  135. Aguilar J, Cameron TA, Zupan J, Zambryski P (2011) Membrane and core periplasmic Agrobacterium tumefaciens virulence type IV secretion system components localize to multiple sites around the bacterial perimeter during lateral attachment to plant cells. MBio 2:e00218–e00211. https://doi.org/10.1128/mBio.00218-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Kegler H, Fuchs E, Plescher A, Ehrig F, Schliephake E, Grüntzig M (1999) Evidence and characterization of a virus of St John’s wort (Hypericum perforatum L.). Arch Phytopathol Plant Prot 32:205–221. https://doi.org/10.1080/03235409909383290

    Article  Google Scholar 

  137. Du Z, Tang Y, Zhang S, She X, Lan G, Varsani A, He Z (2013) Identification and molecular characterization of a single-stranded circular DNA virus with similarities to Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1. Arch Virol 159:1527–1531. https://doi.org/10.1007/s00705-013-1890-5

    Article  CAS  PubMed  Google Scholar 

  138. Rai M, Bansod S, Bawaskar M, Gade A, Santos CA, Seabra AB et al (2015) Nanoparticles-based delivery systems in plant genetic transformation. In: Rai M, Ribeiro C, Mattoso L, Duran N (eds) Nanotechnologies in food and agriculture. Springer International Publishing, Cham, pp 209–239

    Google Scholar 

  139. Soták M, Czeranková O, Klein D, Nigutová K, Altschmied L, Li L et al (2016) Differentially expressed genes in hypericin-containing Hypericum perforatum leaf tissues as revealed by de novo assembly of RNA-Seq. Plant Mol Biol Rep 34(5):1027–1041. https://doi.org/10.1007/s11105-016-0982-2

    Article  CAS  Google Scholar 

  140. Morshedloo MR, Nabizadeh M, Akramian M, Yazdani D (2017) Characterization of the volatile oil compositions from Hypericum perforatum L. shoot cultures in different basal media. Azarian J Agric 4(1):7–11

    Google Scholar 

  141. Linsmaier EM, Skoog F (1965) Organic growth factor requirements of tobacco tissue cultures. Physiol Plant 18:100–127. https://doi.org/10.1111/j.1399-3054.1965.tb06874.x

    Article  CAS  Google Scholar 

  142. Zobayed SMA, Murch SJ, Rupasinghe HPV, Saxena PK (2003) In vitro production and chemical characterization of St. John’s wort (Hypericum perforatum L. cv ‘New Stem’). Plant Sci 166(2):333–340. https://doi.org/10.1016/j.plantsci.2003.10.005

    Article  CAS  Google Scholar 

  143. Matzk F, Hammer K, Schubert I (2003) Coevolution of apomixis and genome size within the genus Hypericum. Sex Plant Reprod 16:51–58

    Article  Google Scholar 

  144. Ernst E (2003) Hypericum: the genus Hypericum. CRC Press, p 256. isbn:9780415369541

    Google Scholar 

  145. Čellárová E, Kimakova K, Brutovska R (1992) Multiple shoot formation and phenotypic changes of Ro regenerants in Hypericum perforatum L. Acta Biotech 12:445e452. https://doi.org/10.1002/abio.370120602

    Article  Google Scholar 

  146. Franklin G, Dias ACP (2006) Organogenesis and embryogenesis in several Hypericum perforatum genotypes. In Vitro Cell Dev Biol Plant 42:324–330. https://doi.org/10.1079/IVP2006787

    Article  CAS  Google Scholar 

  147. Košuth J, Koperdáková J, Tolonen A, Hohtola A, Ćellárova E (2003) The content of hypericins and phloroglucinols in Hypericum perforatum L. seedlings at early stage of development. Plant Sci 165(3):515–521. https://doi.org/10.1016/S0168-9452(03)00210-3

    Article  CAS  Google Scholar 

  148. Akhtar NF, Aharizad S, Mohammadi SA, Motallebi-Azar A, Movafeghi A, Khojasteh SMB (2013) In vitro shoot regeneration and hypericin production in four Hypericum perforatum L. Genotypes Int J Agric Res Rev 3(4):887–893

    CAS  Google Scholar 

  149. Kwiecień I, Szydłowska A, Kawka B, Beerhues L, Ekiert H (2015) Accumulation of biologically active phenolic acids in agitated shoot cultures of three Hypericum perforatum cultivars: ‘Elixir’, ‘Helos’ and ‘Topas’. Plant Cell Tissue Organ Cult 123(2):273–281. https://doi.org/10.1007/s11240-015-0830-3

    Article  CAS  Google Scholar 

  150. Alan AR, Murch SJ, Saxena PK (2015) Evaluation of ploidy variations in Hypericum perforatum L. (St. John’s wort) germplasm from seeds, in vitro germplasm collection, and regenerants from floral cultures. In Vitro Cell Dev Biol Plant 51(4):452–462. https://doi.org/10.1007/s11627-015-9708-7

    Article  CAS  Google Scholar 

  151. Butiuc-Keul A, Farkas A, Cristea V (2016) Genetic stability assessment of in vitro plants by molecular markers. Studia Universitatis Babeş-Bolyai Biologia 61(1):107–114. http://studia.ubbcluj.ro/download/pdf/Biologia_pdf/2016_1/28.pdf

    Google Scholar 

  152. Morshedloo MR, Ebadi A, Maggi F, Fattahi R, Yazdani D, Jafari M (2015) Chemical characterization of the essential oil compositions from Iranian populations of Hypericum perforatum L. Ind Crops Prod 76:565–573. https://doi.org/10.1016/j.indcrop.2015.07.033

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by a grant of the Ministry of Research and Innovation through Program 1 – Development of the National R&D System Subprogram 1.2 – Institutional Performance – Projects for Excellence Financing in RDI ctr. no. 22PFE/2018 and partially by the core program PN2019-2022 – BIODIVERS 3 through the project BIOSERV project code 19270201 contract nr. 25 N/2019.

Author information

Author notes

  1. All authors made equal contribution in this work and are equally considered as first authors.

Authors and Affiliations

  1. Department of Experimental Biology and Biochemistry, Institute of Biological Research Cluj-Napoca, Cluj-Napoca, România

    Ana Coste & Adela Halmagyi

  2. Department of Drug Industry and Pharmaceutical Biotechnology, Faculty of Pharmacy, University of Medicine & Pharmacy “Iuliu Haţieganu” Cluj-Napoca, Cluj-Napoca, România

    Carmen Pop

  3. Department of Molecular Biology and Biotechnology, Faculty of Biology and Geology, Babeş-Bolyai University, Cluj-Napoca, România

    Anca Butiuc-Keul

Authors
  1. Ana Coste
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carmen Pop
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adela Halmagyi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anca Butiuc-Keul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ana Coste or Carmen Pop .

Editor information

Editors and Affiliations

  1. Department of Botany, M.L.Sukhadia university, Udaipur, Rajasthan, India

    Kishan Gopal Ramawat

  2. Department of Pharmaceutical Botany, Jagiellonian University, Medical College, Kraków, Poland

    Halina Maria Ekiert

  3. Amarillo, TX, USA

    Shaily Goyal

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Coste, A., Pop, C., Halmagyi, A., Butiuc-Keul, A. (2019). Secondary Metabolites in Shoot Cultures of Hypericum. In: Ramawat, K., Ekiert, H., Goyal, S. (eds) Plant Cell and Tissue Differentiation and Secondary Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-030-11253-0_9-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-11253-0_9-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-11253-0

  • Online ISBN: 978-3-030-11253-0

  • eBook Packages: Springer Reference Chemistry and Mat. ScienceReference Module Physical and Materials ScienceReference Module Chemistry, Materials and Physics

Publish with us

Policies and ethics

Search

Navigation