State of antioxidant systems and phenolic compounds’ production in Hypericum perforatum L. hairy roots

• Autorzy: Tusevski O. , Petreska-Stanoeva J. , Stefova M. , Spasenoski M. , Gadzovska-Simic S.
• Języki publikacji: EN

Abstrakty

EN

Hypericum perforatum hairy root clones (HR A–HR O) transformed with Agrobacterium rhizogenes A4 were evaluated for growth characteristics, phenolic compounds production, antioxidant/radical scavenging activity, antioxidant enzymes, and oxidative stress markers. The screening of growth characteristics revealed that HR clones were characterized with higher biomass accumulation, root elongation, and lateral branching in comparison to non-transformed roots. Significant increase of phenolics production in HR clones was related to phenylalanine ammonia lyase activity indicating an up-regulation of phenylpropanoid/flavonoid metabolism. Positive correlation of phenolics, flavonoids, and tannins with antioxidant assays indicated that these secondary metabolites significantly contributed to the antioxidant/radical scavenging properties of HR cultures. Regarding the enzymatic antioxidant state, an enhancement of superoxide dismutase activity in HR lines coincided with decrease in O₂˙⁻ production rate, while ascorbate peroxidase and catalase greatly contributed to the reduction of H₂O₂ levels. The substantial accumulation of malondialdehyde in HR clones indicated an efficiency of antioxidant enzymes to reduce O₂˙⁻ and H₂O₂ at levels that are not deleterious for membrane lipids. These results confirmed the involvement of an efficient antioxidant defense system in the response adjustment of H. perforatum HR cultures to transformation process. Two superior clones denoted as HR B and HR F were selected as fast-growing and high biomass yielding lines with up-regulated phenolic compounds’ production, antioxidant, and radical scavenging activity. Altogether, the best performing H. perforatum HR clones could be proposed as a prospective biotechnological system for scale-up production of antioxidant phenolic compounds.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 08
• Opis fizyczny: Article 132 [15p.], fig.,ref.

Twórcy

autor

Tusevski O.

• Institute of Biology, Faculty of Natural Sciences and Mathematics, University „Ss. Cyril and Methodius“, Archimedova str. 3, 1000 Skopje, Macedonia

autor

Petreska-Stanoeva J.

• Institute of Chemistry, Faculty of Natural Sciences and Mathematics, University „Ss. Cyril and Methodius“, Archimedova str. 3, 1000 Skopje, Macedonia

autor

Stefova M.

• Institute of Chemistry, Faculty of Natural Sciences and Mathematics, University „Ss. Cyril and Methodius“, Archimedova str. 3, 1000 Skopje, Macedonia

autor

Spasenoski M.

• Institute of Biology, Faculty of Natural Sciences and Mathematics, University „Ss. Cyril and Methodius“, Archimedova str. 3, 1000 Skopje, Macedonia

autor

Gadzovska-Simic S.

• Institute of Biology, Faculty of Natural Sciences and Mathematics, University „Ss. Cyril and Methodius“, Archimedova str. 3, 1000 Skopje, Macedonia

Bibliografia

• Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126
• Apak R, Güçlü K, Özyürek M, Karademir SE (2004) Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J Agric Food Chem 52(26):7970–7981
• Bais HP, Ravishankar GA (2003) Synergistic effect of auxins and polyamines in hairy roots of Cichorium intybus L. during growth, coumarin production and morphogenesis. Acta Physiol Plant 25(2):193–208
• Baque MA, Hahn EJ, Paek KY (2010) Growth, secondary metabolite production and antioxidant enzyme response of Morinda citrifolia adventitious root as affected by auxin and cytokinin. Plant Biotechnol Rep 4(2):109–116
• Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254
• Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28(1):25–30
• Bulgakov VP (2008) Functions of rol genes in plant secondary metabolism. Biotechnol Adv 26(4):318–324
• Bulgakov VP, Gorpenchenko TY, Veremeichik GN, Shkryl YN, Tchernoded GK, Bulgakov DV, Aminin DL, Zhuravlev YN (2012) The rolB gene suppresses reactive oxygen species in transformed plant cells through the sustained activation of antioxidant defense. Plant Physiol 158:1371–1381
• Chandra S (2012) Natural plant genetic engineer Agrobacterium rhizogenes: role of T-DNA in plant secondary metabolism. Biotechnol Lett 34(3):407–415
• Chung IM, Rekha K, Rajakumar G, Thiruvengadam M (2016) Production of glucosinolates, phenolic compounds and associated gene expression profiles of hairy root cultures in turnip (Brassica rapa ssp. rapa). 3 Biotech 6(2):175. https://doi.org/10.1007/s13205-016-0492-9
• Cui XH, Murthy HN, Jin YX, Yim YH, Kim JY, Paek KY (2011) Production of adventitious root biomass and secondary metabolites of Hypericum perforatum L. in a balloon type airlift reactor. Bioresour Technol 102(21):10072–10079
• Das JR, Bhat SG, Gowda LR (1997) Purification and characterization of a polyphenol oxidase from the kew cultivar of Indian pineapple fruit. J Agric Food Chem 45(6):2031–2035
• Decker EA, Welch B (1990) Role of ferritin as a lipid oxidation catalyst in muscle food. J Agric Food Chem 38(3):674–677
• Di Guardo A, Cellarova E, Koperdáková J, Pistelli L, Ruffoni B, Allavena A, Giovannini A (2003) Hairy root induction and plant regeneration in Hypericum perforatum L. J Genet Breed 57(3):269–278
• Dilshad E, Zafar S, Ismail H, Waheed MT, Cusido RM, Palazon J, Mirza B (2016) Effect of rol genes on polyphenols biosynthesis in Artemisia annua and their effect on antioxidant and cytotoxic potential of the plant. Appl Biochem Biotechnol 179(8):1456–1468
• Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3(5):371–390
• Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70(2):616–620
• Fathi H, Ebrahimzadeh MA (2013) Antioxidant and free radical scavenging activities of Hypericum perforatum L. (st. John’s wort). Int J For Soil Eros 3(2):68–72
• Fraisse D, Carnat A, Viala D, Pradel P, Besle JM, Coulon JB, Felgines C, Lamaison JL (2007) Polyphenolic composition of a permanent pasture: variations related to the period of harvesting. J Sci Food Agric 87(13):2427–2435
• Franklin G, Conceição LF, Kombrink E, Dias ACP (2008) Hypericum perforatum plant cells reduce Agrobacterium viability during co-cultivation. Planta 227(6):1401–1408
• Franklin G, Conceição LF, Kombrink E, Dias ACP (2009) Xanthone biosynthesis in Hypericum perforatum cells provides antioxidant and antimicrobial protection upon biotic stress. Phytochemistry 70(1):60–68
• 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. https://doi.org/10.1155/2014/609649
• Gadzovska Simic S, Tusevski O, Maury S, Delaunay A, Lainé E, Joseph C, Hagège D (2015a) Polysaccharide elicitors enhance phenylpropanoid and naphtodianthrone production in cell suspension cultures of Hypericum perforatum. Plant Cell Tissue Org 122(3):649–663
• Gadzovska Simic S, Tusevski O, Maury S, Hano C, Delaunay A, Chabbert B, Lamblin F, Lainé E, Joseph C, Hagège D (2015b) Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures. Plant Cell Tissue Org 122(1):213–226
• 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(6):591–601
• Gadzovska S, Maury S, Delaunay A, Spasenoski M, Joseph C, Hagege D (2007) Jasmonic acid elicitation of Hypericum perforatum L. cell suspensions and effects on the production of phenylpropanoids and naphtodianthrones. Plant Cell Tissue Org 89(1):1–13
• 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 Tissue Org 113(1):25–39
• Gadzovska-Simic S, Tusevski O, Antevski S, Atanasova-Pancevska N, Petreska J, Stefova M, Dz Kungulovski, Spasenoski M (2012) Secondary metabolite production in Hypericum perforatum L. cell suspensions upon elicitation with fungal mycelia from Aspergillus flavus. Arch Biol Sci 64(1):113–121
• Gamborg OL, Miller R, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50(1):151–158
• Georgiev VG, Weber J, Kneschke EM, Denev PN, Bley T, Pavlov AI (2010) Antioxidant activity and phenolic content of betalain extracts from intact plants and hairy root cultures of the red beetroot Beta vulgaris cv. Detroit dark red. Plant Foods Hum Nutr 65(2):105–111
• Gupta R, Pandey P, Singh S, Singh DK, Saxena A, Luqman S, Bawankule DU, Banerjee S (2016) Advances in Boerhaavia diffusa: a valuable pursuit for identifying strain sensitivity and up-scaling factors to refine metabolite yield and bioactivity potentials. Protoplasma 253(4):1145–1158
• Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198
• Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55(1):184–185
• Komarovská H, Giovannini A, Košuth J, Čellárová E (2009) Agrobacterium rhizogenes-mediated transformation of Hypericum tomentosum L. and Hypericum tetrapterum Fries. Z Naturforsch C 64(11–12):864–868
• Li YG, Tanner G, Larkin P (1996) The DMACA-HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J Sci Food Agric 70(1):89–101
• Liu F, Ooi VEC, Chang ST (1997) Free radical scavenging activities of mushroom polysaccharide extracts. Life Sci 60(10):763–771
• Liu C, Zhu J, Liu Z, Li L, Pan R, Jin L (2002) Exogenous auxin effects on growth and phenotype of normal and hairy roots of Pueraria lobata (Willd.) Ohwi. Plant Growth Regul 38(1):37–43
• Makris DP, Boskou G, Andrikopoulos NK (2007) Polyphenolic content and in vitro antioxidant characteristics of wine industry and other agri-food solid waste extracts. J Food Compos Anal 20(2):125–132
• Marcocci L, Maguire JJ, Droylefaix MT, Packer L (1994) The nitric oxide-scavenging properties of Ginkgo biloba extract EGb 761. Biochem Biophys Res Commun 201(2):748–755
• Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3):473–497
• Murch SJ, Saxena PK (2006) St. John’s wort (Hypericum perforatum L.): challenges and strategies for production of chemically-consistent plants. Can J Plant Sci 86(3):765–771
• Nahrstedt A, Butterweck V (2010) Lessons learned from herbal medicinal products: the example of St. John’s Wort. J Nat Prod 73(5):1015–1021
• Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880
• Nikravesh F, Khavari-Nejad RA, Rahimian H, Fahimi H (2012) Study of antioxidant enzymes activity and isozymes pattern in hairy roots and regenerated plants in Nicotiana tabacum. Acta Physiol Plant 34(2):419–427
• Orčić DZ, Mimica-Dukić NM, Francišković MM, Petrović SS, Jovin EĐ (2011) Antioxidant activity relationship of phenolic compounds in Hypericum perforatum L. Chem Cent J 5(1):1–8
• Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25(1):223–230
• Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12(1):29–36
• Ruch RJ, Cheng SJ, Klaunig JE (1989) Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 10(6):1003–1008
• Saddiqe Z, Naeem I, Maimoona A (2010) A review of the antibacterial activity of Hypericum perforatum L. J Ethnopharmacol 131(3):511–521
• Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Compt Rend Acad Bulg Sci 51(3):121–124
• Shohael AM, Chakrabarty D, Ali MB, Yu KW, Hahn EJ, Lee HL, Paek KY (2006) Enhancement of eleutherosides production in embryogenic cultures of Eleutherococcus sessiliflorus in response to sucrose-induced osmotic stress. Process Biochem 41(3):512–518
• Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16(3):144–158
• Srivastava S, Conlan XA, Adholeya A, Cahill DM (2016) Elite hairy roots of Ocimum basilicum as a new source of rosmarinic acid and antioxidants. Plant Cell Tissue Org 126(1):19–32
• Tang W, Newton RJ (2004) Increase of polyphenol oxidase and decrease of polyamines correlate with tissue browning in Virginia pine (Pinus virginiana Mill.). Plant Sci 167(3):621–628
• Thiruvengadam M, Praveen N, Kim EH, Kim SH, Chung IM (2014) Production of anthraquinones, phenolic compounds and biological activities from hairy root cultures of Polygonum multiflorum Thunb. Protoplasma 251(3):555–566
• Thwe AA, Kim JK, Li X, Kim YB, Uddin MR, Kim SJ, Suzuki T, Park NI, Park SU (2013) Metabolomic analysis and phenylpropanoid biosynthesis in hairy root culture of tartary buckwheat cultivars. PLoS One 8(6):e65349
• Tiwari RK, Trivedi M, Guang ZC, Guo GQ, Zheng GC (2008) Agrobacterium rhizogenes mediated transformation of Scutellaria baicalensis and production of flavonoids in hairy roots. Biol Plantarum 52(1):26–35
• Tusevski O, Petreska Stanoeva J, Stefova M, Gadzovska Simic S (2013a) Phenolic profile of dark-grown and photoperiod-exposed Hypericum perforatum L. hairy root cultures. Sci World J. https://doi.org/10.1155/2013/602752
• Tusevski O, Stanoeva J, Stefova M, Kungulovski D, Pancevska N, Sekulovski N, Panov S, Gadzovska Simic S (2013b) Hairy roots of Hypericum perforatum L.: a promising system for xanthone production. Open Life Sci 8(10):1010–1022
• Tusevski O, Stanoeva JP, 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
• 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
• Tusevski O, Stanoeva JP, Markoska E, Brndevska N, Stefova M, Gadzovska Simic S (2016) Callus cultures of Hypericum perforatum L. a novel and efficient source for xanthone production. Plant Cell Tissue Org 125(2):309–319
• Tusevski O, Vinterhalter B, Milošević DK, Soković M, Ćirić A, Vinterhalter D, Zdravković Korać S, Petreska Stanoeva J, Stefova M, Gadzovska Simic S (2017) Production of phenolic compounds, antioxidant and antimicrobial activities in hairy root and shoot cultures of Hypericum perforatum L. Plant Cell Tiss Org 128(3):589–605
• Vinterhalter B, Ninković S, Cingel A, Vinterhalter D (2006) Shoot and root culture of Hypericum perforatum L. transformed with Agrobacterium rhizogenes A4M70GUS. Biol Plantarum 50(4):767–770
• Vinterhalter B, Zdravković-Korać S, Mitić N, Bohanec B, Vinterhalter D, Savić J (2015) Effect of sucrose on shoot regeneration in Agrobacterium transformed Hypericum perforatum L. roots. Acta Physiol Plant 37(2):1–12
• Wang JW, Zheng LP, Zhang B, Zou T (2009) Stimulation of artemisinin synthesis by combined cerebroside and nitric oxide elicitation in Artemisia annua hairy roots. Appl Microbiol Biotechnol 85(2):285–292
• Weremczuk-Jeżyna I, Grzegorczyk-Karolak I, Frydrych B, Królicka A, Wysokińska H (2013) Hairy roots of Dracocephalum moldavica: rosmarinic acid content and antioxidant potential. Acta Physiol Plant 35(7):2095–2103
• Xu MJ, Dong JF, Zhu MY (2005) Nitric oxide mediates the fungal elicitor-induced hypericin production of Hypericum perforatum cell suspension cultures through a jasmonic-acid-dependent signal pathway. Plant Physiol 139(2):991–998
• 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(11):1953–1962

Identyfikatory

DOI

10.1007/s11738-019-2919-5