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

Plant Cell Reports

Volumn 35, Issue 5, 2016, Pages 1009-1020

  Valletta, Alessio ^a   De Angelis, Giulia ^a   Badiali, Camilla ^a   Brasili, Elisa ^a   Miccheli, Alfredo ^a   Di Cocco, Maria Enrica ^a   Pasqua, Gabriella ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Acetic acid; Chitosan; Elicitor; Hypericum perforatum; Root cultures; Xanthones

Indexed keywords

ACETIC ACID; CARBOXYLIC ACID; CHITOSAN; XANTHONE; XANTHONE DERIVATIVE;

DRUG EFFECTS; HYPERICUM; METABOLISM; PLANT ROOT; SIGNAL TRANSDUCTION;

ACETIC ACID; CARBOXYLIC ACIDS; CHITOSAN; HYPERICUM; PLANT ROOTS; SIGNAL TRANSDUCTION; XANTHONES;

EID: 84955266223     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-016-1934-x     Document Type: Article

References (45)

1. Abd El-Mawla AMA, Beerhues L (2002) Benzoic acid biosynthesis in cell cultures of Hypericum androsaemum. Planta 214:727–733
2. 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
3. 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
4. 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
5. 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
6. 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
7. 1H-NMR based metabolomics associated with ASCA modelling. Plant Biosyst (Submitted)
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. European Pharmacopoeia (2008) St. John’s wort. In: European Pharmacopoeia (6th edn). Strasbourg, France: Council of Europe, 2958–2959
17. Fotie J, Bohle DS (2006) Pharmacological and biological activities of xanthones. Anti-Infect Agents Med Chem 5:15–31
18. 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
19. Gagnon H, Ibrahim RK (1997) Effects of various elicitors on the accumulation and secretion of isoflavonoids in white lupin. Phytochemistry 44:1463–1467
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. Masters KS, Bräse S (2012) Xanthones from fungi, lichens, and bacteria: the natural products and their synthesis. Chem Rev 112:3717–3776
27. Müller WE (2003) Current St. John’s wort research from mode of action to clinical efficacy. Pharmacol Res 47:101–109
28. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
29. 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
30. 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
31. 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
32. 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
33. Schmidt W, Beerhues L (1997) Alternative pathways of xanthone biosynthesis in cell cultures of Hypericum androsaemum L. FEBS Lett 420:143–146
34. 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
35. 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
36. 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
37. 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
38. 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
39. 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
40. 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
41. 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
42. 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
43. 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
44. 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
45. 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