Skip to main content
SpringerLink
Log in

Acetic acid acts as an elicitor exerting a chitosan-like effect on xanthone biosynthesis in Hypericum perforatum L. root cultures

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Acetic acid acts as a signal molecule, strongly enhancing xanthone biosynthesis in Hypericum perforatum root cultures. This activity is specific, as demonstrated by the comparison with other short-chain monocarboxylic acids.

Abstract

We have recently demonstrated that Hypericum perforatum root cultures constitutively produce xanthones at higher levels than the root of the plant and that they respond to chitosan (CHIT) elicitation with a noteworthy increase in xanthone production. In the present study, CHIT was administered to H. perforatum root cultures using three different elicitation protocols, and the increase in xanthone production was evaluated. The best results (550 % xanthone increase) were obtained by subjecting the roots to a single elicitation with 200 mg l−1 CHIT and maintaining the elicitor in the culture medium for 7 days. To discriminate the effect of CHIT from that of the solvent, control experiments were performed by administering AcOH alone at the same concentration used for CHIT solubilization. Unexpectedly, AcOH caused an increase in xanthone production comparable to that observed in response to CHIT. Feeding experiments with 13C-labeled AcOH demonstrated that this compound was not incorporated into the xanthone skeleton. Other short-chain monocarboxylic acids (i.e., propionic and butyric acid) have little or no effect on the production of xanthones. These results indicate that AcOH acts as a specific signal molecule, able to greatly enhance xanthone biosynthesis in H. perforatum root cultures.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abd El-Mawla AMA, Beerhues L (2002) Benzoic acid biosynthesis in cell cultures of Hypericum androsaemum. Planta 214:727–733

    Article  CAS  PubMed  Google Scholar 

  • Abraham F, Bhatt A, Keng CL, Indrayanto G, Sulaiman SF (2013) Effect of yeast extract and chitosan on shoot proliferation, morphology and antioxidant activity of Curcuma mangga in vitro plantlets. Afr J Biotechnol 10:7787–7795

    Google Scholar 

  • Ahmed SA, Baig MMV (2014) Biotic elicitor enhanced production of psoralen in suspension cultures of Psoralea corylifolia L. Saudi J Biol Sci 21:499–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong J, Armstrong W (2001) Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. Am J Bot 88:1359–1370

    Article  CAS  PubMed  Google Scholar 

  • Beerhues L, Liu B (2009) Biosynthesis of biphenyls and benzophenones: evolution of benzoic acid-specific type III polyketide synthases in plants. Phytochemistry 70:1719–1727

    Article  CAS  PubMed  Google Scholar 

  • Brasili E, Praticò G, Marini F, Valletta A, Capuani G, Sciubba F, Miccheli A, Pasqua G (2014) A non-targeted metabolomics approach to evaluate the effects of biomass growth and chitosan elicitation on primary and secondary metabolism of Hypericum perforatum in vitro roots. Metabolomics 10:1186–1196

    Article  CAS  Google Scholar 

  • Brasili E, Miccheli A, Marini F, Praticò G, Sciubba F, Di Cocco ME, Cechinel Filho V, Tocci N, Valletta A, Pasqua G (2015) A time-dependent metabolic response to high biomass density and chitosan elicitation in Hypericum perforatum in vitro roots as revealed by 1H-NMR based metabolomics associated with ASCA modelling. Plant Biosyst (Submitted)

  • Chang LH, Shin JH, Chung IS, Lee HJ (1998) Improved menthol production from chitosan-elicited suspension culture of Mentha piperita. Biotechnol Lett 20:1097–1099

    Article  CAS  Google Scholar 

  • Ciggin AS, Orthon D, Capitani D, Miccheli A, Puccetti C, Majone M (2013) Aerobic metabolism of mixed carbon sources in sequencing batch reactor under pulse and continuous feeding. Bioresour Techonol 129:118–126

    Article  CAS  Google Scholar 

  • Conceição LF, Ferreres F, Tavares RM, Dias AC (2006) Induction of phenolic compounds in Hypericum perforatum L. cells by Colletotrichum gloeosporioides elicitation. Phytochemistry 67:149–155

    Article  PubMed  Google Scholar 

  • Conrad R, Klose M (1999) Anaerobic conversion of carbon dioxide to methane, acetate and propionate on washed rice roots. FEMS Microbiol Ecol 30:147–155

    Article  CAS  PubMed  Google Scholar 

  • Crockett SL, Poller B, Tabanca N, Pferschy-Wenzig EM, Kunert O, Wedge DE, Bucar F (2011) Bioactive xanthones from the roots of Hypericum perforatum (common St John’s wort). J Sci Food Agr 91:428–434

    Article  CAS  Google Scholar 

  • Cui XH, Chakrabarty D, Lee AJ, Paek KY (2010) Production of adventitious roots and secondary metabolites by Hypericum perforatum L. in a bioreactor. Bioresour Techonol 101:4708–4716

    Article  CAS  Google Scholar 

  • Dionisi D, Majone M, Miccheli A, Puccetti C, Sinisi C (2004) Glutamic acid removal and PHB storage in the activated sludge process under dynamic conditions. Biotechnol Bioeng 86:842–851

    Article  CAS  PubMed  Google Scholar 

  • El-Seedi HR, El-Ghorab DM, El-Barbary MA, Zayed MF, Goransson U, Larsson S, Verpoorte R (2009) Naturally occurring xanthones; latest investigations: isolation, structure elucidation and chemosystematic significance. Curr Med Chem 16:2581–2626

    Article  CAS  PubMed  Google Scholar 

  • European Pharmacopoeia (2008) St. John’s wort. In: European Pharmacopoeia (6th edn). Strasbourg, France: Council of Europe, 2958–2959

  • Fotie J, Bohle DS (2006) Pharmacological and biological activities of xanthones. Anti-Infect Agents Med Chem 5:15–31

    Article  CAS  Google Scholar 

  • Franklin G, Conceição LF, Kombrink E, Dias AC (2009) Xanthone biosynthesis in Hypericum perforatum cells provides antioxidant and antimicrobial protection upon biotic stress. Phytochemistry 70:60–68

    Article  CAS  PubMed  Google Scholar 

  • Gagnon H, Ibrahim RK (1997) Effects of various elicitors on the accumulation and secretion of isoflavonoids in white lupin. Phytochemistry 44:1463–1467

    Article  CAS  Google Scholar 

  • Gaid MM, Sircar D, Müller A, Beuerle T, Liu B, Ernst L, Hänsch R, Beerhues L (2012) Cinnamate: CoA ligase initiates biosynthesis of a benzoate-derived xanthone phytoalexin in Hypericum calycinum cell cultures. Plant Physiol 160:1267–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorietti D, Zanni E, Palleschi C, Delfini M, Uccelletti D, Saliola M, Puccetti C, Sobolev AP, Mannina L, Miccheli A (2015) 13C NMR based profiling unveils different α-ketoglutarate pools involved into glutamate and lysine synthesis in the milk yeast Kluyveromyces lactis. BBA-Gen Subjects 1850:2222–2227

    Article  CAS  Google Scholar 

  • Koyama H, Toda T, Hara T (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin–Ca interaction may play an important role in proton rhizotoxicity. J Exp Bot 52:361–368

    Article  CAS  PubMed  Google Scholar 

  • Lecrubier Y, Clerc G, Didi R, Kieser M (2002) Efficacy of St. John’s wort extract WS 5570 in major depression: a double-blind, placebo-controlled trial. Am J Psychiatr 159(8):1361–1366

    Article  CAS  PubMed  Google Scholar 

  • Malik S, Bhushan S, Verma SC et al (2008) Production of naphthoquinone pigments in cell suspension cultures of Arnebia euchroma (Royle) Johnston: influence of pH on growth kinetics and acetylshikonin. Med Aromat Plant Sci Biotechnol 2:43–49

    Google Scholar 

  • Malik S, Bhushan S, Sharma M, Ahuja PS (2014) Biotechnological approaches to the production of shikonins: a critical review with recent updates. Crit Rev Biotechnol. doi:10.3109/07388551.2014.961003

    PubMed  Google Scholar 

  • Masters KS, Bräse S (2012) Xanthones from fungi, lichens, and bacteria: the natural products and their synthesis. Chem Rev 112:3717–3776

    Article  CAS  PubMed  Google Scholar 

  • Müller WE (2003) Current St. John’s wort research from mode of action to clinical efficacy. Pharmacol Res 47:101–109

    Article  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Ndimba BK, Chivasa S, Hamilton JM, Simon WJ, Slabas AR (2003) Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 3:1047–1059

    Article  CAS  PubMed  Google Scholar 

  • Patil RA, Lenka SK, Normanly J, Walker EL, Roberts SC (2014) Methyl jasmonate represses growth and affects cell cycle progression in cultured Taxus cells. Plant Cell Rep 33:1479–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pitta-Alvarez SI, Giulietti AM (1999) Influence of chitosan, acetic acid and citric acid on growth and tropane alkaloid production in transformed roots of Brugmansia candida: effect of medium pH and growth phase. Plant Cell Tissue Organ 59:31–38

    Article  CAS  Google Scholar 

  • Santamaria AR, Mulinacci N, Valletta A, Innocenti M, Pasqua G (2011) Effects of elicitors on the production of resveratrol and viniferins in cell cultures of Vitis vinifera L. cv Italia. J Agric Food Chem 59:9094–9101

    Article  CAS  PubMed  Google Scholar 

  • Schmidt W, Beerhues L (1997) Alternative pathways of xanthone biosynthesis in cell cultures of Hypericum androsaemum L. FEBS Lett 420:143–146

    Article  CAS  PubMed  Google Scholar 

  • Simonetti G, Tocci N, Valletta A, Brasili E, D’Auria FD, Idoux A, Pasqua G (2015) In vitro antifungal activity of extracts obtained from Hypericum perforatum adventitious roots cultured in a mist bioreactor against planktonic cells and biofilm of Malassezia furfur. Nat Prod Res 13:1–7

    Google Scholar 

  • Sun J, Xiao J, Wang X, Yuan X, Zhao B (2012) Improved cardenolide production in Calotropis gigantea hairy roots using mechanical wounding and elicitation. Biotechnol Lett 34:563–569

    Article  CAS  PubMed  Google Scholar 

  • Tocci N, Ferrari F, Santamaria AR, Valletta A, Rovardi I, Pasqua G (2010) Chitosan enhances xanthone production in Hypericum perforatum subsp. angustifolium cell cultures. Nat Prod Res 24:286–293

    Article  CAS  PubMed  Google Scholar 

  • Tocci N, Simonetti G, D’Auria FD, Panella S, Palamara AT, Valletta A, Pasqua G (2011) Root cultures of Hypericum perforatum subsp. angustifolium elicited with chitosan and production of xanthone-rich extracts with antifungal activity. Appl Microbiol Biotechnol 91:977–987

    Article  CAS  PubMed  Google Scholar 

  • Tocci N, D’Auria FD, Simonetti G, Panella S, Palamara AT, Pasqua G (2012) A three-step culture system to increase the xanthone production and antifungal activity of Hypericum perforatum subsp. angustifolium in vitro roots. Plant Physiol Biochem 57:54–58

    Article  CAS  PubMed  Google Scholar 

  • Tocci N, Simonetti G, D’Auria FD, Penella A, Palamara AT, Ferrari F, Pasqua G (2013) Chemical composition and antifungal activity of Hypericum perforatum subsp. angustifolium roots from wild plants and plants grown under controlled conditions. Plant Biosyst 147:557–562

    Article  Google Scholar 

  • Tusevski O, Stanoeva JP, Stefova M, Kungulovski D, Pancevska NA, Sekulovski N, Panov S, Gadzovska Simic S (2013) Hairy roots of Hypericum perforatum L.: a promising system for xanthone production. Cent Eur J Biol 8:1010–1022

    CAS  Google Scholar 

  • Udomsuk L, Jarukamjorn K, Tanaka H, Putalun W (2011) Improved isoflavonoid production in Pueraria candollei hairy root cultures using elicitation. Biotechnol Lett 33:369–374

    Article  CAS  PubMed  Google Scholar 

  • Valletta A, Santamaria AR, Canini A, Canuti L, Pasqua G (2013) Trichomes in Camptotheca acuminata Decaisne (Nyssaceae): morphology, distribution, structure, and secretion. Plant Biosyst 147:548–556

    Article  Google Scholar 

  • Xu A, Zhan JC, Huang WD (2015) Combined elicitation of chitosan and ultraviolet C enhanced stilbene production and expression of chitinase and β-1,3-glucanase in Vitis vinifera cell suspension cultures. Plant Cell Tissue Org. doi:10.1007/s11240-015-0879-z

    Google Scholar 

  • Zobayed SMA, Murcha SJ, Rupasingheb HPV, Saxena PK (2004) In vitro production and chemical characterization of St. John’s wort (Hypericum perforatum L. cv ‘New Stem’). Plant Sci 166:333–340

    Article  CAS  Google Scholar 

  • Zubrická D, Mišianiková A, Henzelyová J, Valletta A, De Angelis G, D’Auria FD, Simonetti G, Pasqua G, Čellárová E (2015) Xanthones from roots, hairy roots and cell suspension cultures of selected Hypericum species and their antifungal activity against Candida albicans. Plant Cell Rep 34:1953–1962

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Sapienza Università di Roma (Ricerche Universitarie 2014, Grant Number C26A14RP98).

Author information

Authors and Affiliations

  1. Department of Environmental Biology, Sapienza University of Rome, Rome, Italy

    Alessio Valletta, Giulia De Angelis, Camilla Badiali, Elisa Brasili & Gabriella Pasqua

  2. Department of Chemistry, Sapienza University of Rome, Rome, Italy

    Alfredo Miccheli & Maria Enrica Di Cocco

Authors
  1. Alessio Valletta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giulia De Angelis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camilla Badiali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisa Brasili
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alfredo Miccheli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Enrica Di Cocco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gabriella Pasqua
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alessio Valletta.

Ethics declarations

Conflict of interest

The author(s) declare that they have no competing interests.

Additional information

Communicated by M. Petersen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 76 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valletta, A., De Angelis, G., Badiali, C. et al. Acetic acid acts as an elicitor exerting a chitosan-like effect on xanthone biosynthesis in Hypericum perforatum L. root cultures. Plant Cell Rep 35, 1009–1020 (2016). https://doi.org/10.1007/s00299-016-1934-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1934-x

Keywords

Search

Navigation