Skip to main content
SpringerLink
Log in

Effects of yeast extract on the production of phenylpropanoid metabolites in callus culture of purple basil (Ocimum Basilicum L. var purpurascens) and their in-vitro evaluation for antioxidant potential

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Ocimum basilicum L. var. purpurascens is an enriched reservoir of pharmaceutically important compounds with plenty of health and therapeutic attributes such as phenolic acids and anthocyanins. However, the inefficient production of aforementioned metabolites in wild has restricted its commercial utilization. Herein, commercially viable phytochemicals have been enhanced through elicitation of in-vitro cultures of O. basilicum using yeast extract.The impact of various concentrations (YE 1 mg/L,YE 10 mg/L, YE 25 mg/L, YE 50 mg/L, YE 100 mg/L, YE 200 mg/L and YE 400 mg/L) of yeast extract on biomass accumulation, phytochemical production, and antioxidant activities were assessed in callus cultures. Moderate concentration of yeast extract (100 mg/L) enhanced biomass accumulation i.e. fresh weight (FW 216.28 g/L) and dry weight (DW 15.49 g/L) up to 1.5 folds as compared to control (FW 167.14 g/L and DW 10.25 g/L). Similarly, yeast extract (100 mg/L) increased total phenolic and flavonoid contents as well as enhanced antioxidant activities such as ABTS (2,2 azinobis 3-ethylbenzthiazoline-6-sulphonic acid), FRAP (ferric reducing antioxidant power) and DPPH (2,2-diphenyl-1-picryhydrazyl). High performance liquid chromatography (HPLC) analysis was elucidated for further phytochemical investigation. HPLC analysis showed an increase of almost 1.9 folds as compared to control in rosmarinic acid (15.19 mg/g DW), chicoric acid (2.13 mg/g DW), peonidin (2.70 mg/g DW) and cyanidin (1.57 mg/g DW). Likewise, 1.8 fold and 2.4 folds increase was observed in eugenol essential oils (0.25 mg/g DW) and chavicol (0.037 mg/g DW), respectively. For cellular antioxidant activity, reactive oxygen specie or reactive nitogen specie (ROS/RNS) was induced in yeast cells and the effect of O. basilicum callus culture was further investigated in stressed yeast cells. A positive correlation exists between the antioxidant activities, TPC and TFC analysis. In short, these results showed that yeast extract could act as an efficient elicitor to enhance pharmacologically important metabolites in callus cultures of Ocimum basilicum.

Graphical abstract

Key message

Yeast-enhanced biosynthesis of phenylpropanoid metabolism in the callus cultures of Ocimum basilicum.

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

Abbreviations

MS:

Murashige and Skoog

DPPH:

2,2-Diphenyl-1-picryhydrazyl

FRAP:

Ferric reducing antioxidant power

ABTS:

2,2-Azinobis 3-ethybenzthiazoine-6-suphonic acid

NAA:

α-Napthalene acetic acid

DMSO:

Dimethyl sulfoxide

HPLC:

High performance liquid chromatography

DW:

Dry weight

FW:

Fresh weight

TFP:

Total flavonoid production

TFC:

Total flavonoid content

TFP:

Total phenol production

TPC:

Total phenol content

RA:

Rosmarinic acid

TEAC:

Trolox C equivalent antioxidant capacity

References

  • Abraham F, Bhatt A, Keng CL, Indrayanto G, Sulaiman SF (2011) Effect of yeast extract and chitosan on shoot proliferation, morphology and antioxidant activity of Curcuma mangga in vitro plantlets. Afr J Biotech 10(40):7787–7795

    Article  CAS  Google Scholar 

  • Açıkgöz MA (2020) Establishment of cell suspension cultures of Ocimum basilicum L. and enhanced production of pharmaceutical active ingredients. Ind Crops Prod 148:112278

    Article  CAS  Google Scholar 

  • Ali MB, Khatun S, Hahn E-J, Paek K-Y (2006) Enhancement of phenylpropanoid enzymes and lignin in Phalaenopsis orchid and their influence on plant acclimatisation at different levels of photosynthetic photon flux. Plant Growth Regul 49(2–3):137–146

    Article  CAS  Google Scholar 

  • Ames BN, Shigenaga MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci 90(17):7915–7922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baenas N, García-Viguera C, Moreno DA (2014) Elicitation: a tool for enriching the bioactive composition of foods. Molecules 19(9):13541–13563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76

  • Berim A, Gang DR (2020) Extractability, stability, and accumulation of nepetoidins in Ocimum basilicum L. leaves and cell cultures. Plant Cell Tiss Organ Cult 143(1):75–85

    Article  CAS  Google Scholar 

  • Bertoli A, Lucchesini M, Mensuali-Sodi A, Leonardi M, Doveri S, Magnabosco A, Pistelli L (2013) Aroma characterisation and UV elicitation of purple basil from different plant tissue cultures. Food Chem 141(2):776–787

    Article  CAS  PubMed  Google Scholar 

  • Cakir O, Ari S (2009) Defensive and secondary metabolism in Astragalus chrysochlorus cell cultures, in response to yeast extract stressor. J Environ Biol 30(1):51–55

    PubMed  Google Scholar 

  • Chiang LC, Ng LT, Cheng PW, Chiang W, Lin CC (2005) Antiviral activities of extracts and selected pure constituents of Ocimum basilicum. Clin Exp Pharmacol Physiol 32(10):811–816

    Article  CAS  PubMed  Google Scholar 

  • Christie JM, Jenkins GI (1996) Distinct UV-B and UV-A/blue light signal transduction pathways induce chalcone synthase gene expression in Arabidopsis cells. Plant Cell 8(9):1555–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duran RE, Kilic S, Coskun Y (2019) Melatonin influence on in vitro callus induction and phenolic compound production in sweet basil (Ocimum basilicum L.). In Vitro Cell Dev Biol Plant 55(4):468–475

    Article  CAS  Google Scholar 

  • El-Nabarawy M, El-Kafafi S, Hamza M, Omar M (2015) The effect of some factors on stimulating the growth and production of active substances in Zingiber officinale callus cultures. Ann Agric Sci 60(1):1–9

    Article  Google Scholar 

  • Ge X, Wu J (2005) Tanshinone production and isoprenoid pathways in Salvia miltiorrhiza hairy roots induced by Ag+ and yeast elicitor. Plant Sci 168(2):487–491

  • George EF, Hall MA, De Klerk G-J (2008) The components of plant tissue culture media II: organic additions, osmotic and pH effects, and support systems Plant propagation by tissue culture. Springer, Dordrecht, pp 115–173

    Google Scholar 

  • Goel MK, Mehrotra S, Kukreja AK (2011) Elicitor-induced cellular and molecular events are responsible for productivity enhancement in hairy root cultures: an insight study. Appl Biochem Biotechnol 165(5–6):1342–1355

    Article  CAS  PubMed  Google Scholar 

  • Hussain AI, Anwar F, Sherazi STH, Przybylski R (2008) Chemical composition, antioxidant and antimicrobial activities of basil (Ocimum basilicum) essential oils depends on seasonal variations. Food Chem 108(3):986–995

    Article  CAS  PubMed  Google Scholar 

  • Hussain MS, Fareed S, Saba Ansari M, Rahman A, Ahmad IZ, Saeed M (2012) Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 4(1):10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kalidass C, Mohan VR, Daniel A (2009) Effect of auxin and cytokinin on vincristine production by callus cultures of Catharanthus roseus L.(apocynaceae). Trop Subtrop Agroecos 12(2):283–288

    Google Scholar 

  • Kéita SM, Vincent C, Schmit J-P, Arnason JT, Bélanger A (2001) Efficacy of essential oil of Ocimum basilicum L. and O. gratissimum L. applied as an insecticidal fumigant and powder to control Callosobruchus maculatus (Fab.)[Coleoptera: Bruchidae]. J Stored Prod Res 37(4):339–349

    Article  PubMed  Google Scholar 

  • Khan H, Khan T, Ahmad N, Zaman G, Khan T, Ahmad W, Batool S, Hussain Z, Drouet S, Hano C (2021) Chemical elicitors-induced variation in cellular biomass, biosynthesis of secondary cell products, and antioxidant system in callus cultures of Fagonia indica. Molecules 26(21):6340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khurshid R, Ullah MA, Tungmunnithum D, Drouet S, Shah M, Zaeem A, Hameed S, Hano C, Abbasi BH (2020) Lights triggered differential accumulation of antioxidant and antidiabetic secondary metabolites in callus culture of Eclipta alba L. PLoS One 15(6):e0233963

  • Kikowska M, Kędziora I, Krawczyk A, Thiem B (2015) Methyl jasmonate, yeast extract and sucrose stimulate phenolic acids accumulation in Eryngium planum L. shoot cultures. Acta Biochim Pol 62(2):197–200

    Article  CAS  PubMed  Google Scholar 

  • Kim HK, Oh S-R, Lee H-K, Huh H (2001) Benzothiadiazole enhances the elicitation of rosmarinic acid production in a suspension culture of Agastache rugosa O Kuntze. Biotechnol Lett 23(1):55–60

    Article  Google Scholar 

  • Lawrencet BM (2001) Essential oils: from agriculture to chemistry. Int J Aromather 10(3–4):82–98

    Article  Google Scholar 

  • Lee J, Scagel CF (2009) Chicoric acid found in basil (Ocimum basilicum L.) leaves. Food Chem 115(2):650–656

    Article  CAS  Google Scholar 

  • Li W, Koike K, Asada Y, Yoshikawa T, Nikaido T (2005) Rosmarinic acid production by Coleus forskohliihairy root cultures. Plant Cell Tiss Organ Cult 80(2):151–155

    Article  CAS  Google Scholar 

  • Mendhulkar VD, Vakil MMA (2013) Elicitation of flavonoids by Salicylic acid and Penicillium expansum in Andrographis paniculata (Burm. f.) Nees cell culture. Res Biotechnol 4(2):1–9

    Google Scholar 

  • Miele M, Dondero R, Ciarallo G, Mazzei M (2001) Methyleugenol in Ocimum basilicum L. Cv. genovese gigante. J Agric food chem 49(1):517–521

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  PubMed  Google Scholar 

  • Moharrami F, Hosseini B, Sharafi A, Farjaminezhad M (2017) Enhanced production of hyoscyamine and scopolamine from genetically transformed root culture of Hyoscyamus reticulatus L. elicited by iron oxide nanoparticles. In Vitro Cell Dev Biol Plant 53(2):104–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194(3):346–352

    Article  CAS  Google Scholar 

  • Muhitch MJ, Fletcher JS (1985) Influence of culture age and spermidine treatment on the accumulation of phenolic compounds in suspension cultures. Plant Physiol 78(1):25–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadeem M, Abbasi BH, Garros L, Drouet S, Zahir A, Ahmad W, Giglioli-Guivarc’h N, Hano C (2018) Yeast-extract improved biosynthesis of lignans and neolignans in cell suspension cultures of Linum usitatissimum L. Plant Cell Tiss Organ Cult 135(2):347–355

    Article  CAS  Google Scholar 

  • Nadeem M, Abbasi BH, Younas M, Ahmad W, Zahir A, Hano C (2019) LED-enhanced biosynthesis of biologically active ingredients in callus cultures of Ocimum basilicum. J Photochem Photobiol B 190:172–178

    Article  CAS  PubMed  Google Scholar 

  • Namdeo A (2007) Plant cell elicitation for production of secondary metabolites: a review. Pharmacogn Rev 1(1):69–79

    CAS  Google Scholar 

  • Nassar MA, El-Segai MU, Azoz SN (2015) Influence of foliar spray with yeast extract on vegetative growth, yield of fresh herb, anatomical structure, composition of volatile oil and seed yield components of basil plant (Ocimum basilicum L.). Int J 3(10):978–993

    CAS  Google Scholar 

  • Nazir M, Tungmunnithum D, Bose S, Drouet S, Garros L, Giglioli-Guivarc’h N, Abbasi BH, Hano C (2019) Differential production of phenylpropanoid metabolites in callus cultures of Ocimum basilicum L. with distinct in vitro antioxidant activities and in vivo protective effects against UV stress. J agric food chem 67(7):1847–1859

    Article  CAS  PubMed  Google Scholar 

  • Nazir S, Jan H, Zaman G, Ahmed N, Drouet S, Hano C, Abbasi BH (2021) Synergistic effects of salicylic acid and light stress on bioactive metabolites in basil callus cultures. Biocatal Agric Biotechnol 37:102176

    Article  CAS  Google Scholar 

  • Nazir S, Jan H, Zaman G, Khan T, Ashraf H, Meer B, Zia M, Drouet S, Hano C, Abbasi BH (2021b) Copper oxide (CuO) and manganese oxide (MnO) nanoparticles induced biomass accumulation, antioxidants biosynthesis and abiotic elicitation of bioactive compounds in callus cultures of Ocimum basilicum (Thai basil). Artif Cells Nanomed Biotechnol 49(1):626–634

    PubMed  CAS  Google Scholar 

  • Opalchenova G, Obreshkova D (2003) Comparative studies on the activity of basil—an essential oil from Ocimum basilicum L.—against multidrug resistant clinical isolates of the genera Staphylococcus, Enterococcus and Pseudomonas by using different test methods. J Microbiol methods 54(1):105–110

    Article  CAS  PubMed  Google Scholar 

  • Pauw B, Van Duijn B, Kijne JW, Memelink J (2004) Activation of the oxidative burst by yeast elicitor in Catharanthus roseus cells occurs independently of the activation of genes involved in alkaloid biosynthesis. Plant Mol Biol 55(6):797–805

    Article  CAS  PubMed  Google Scholar 

  • Petersen M, Simmonds MS (2003) Rosmarinic acid. Phytochemistry 62(2):121–125

    Article  CAS  PubMed  Google Scholar 

  • Petersen M, Abdullah Y, Benner J, Eberle D, Gehlen K, Hücherig S, Janiak V, Kim KH, Sander M, Weitzel C (2009) Evolution of rosmarinic acid biosynthesis. Phytochemistry 70(15–16):1663–1679

    Article  CAS  PubMed  Google Scholar 

  • Phippen WB, Simon JE (1998) Anthocyanins in basil (Ocimum basilicum L.). J Agric Food Chem 46(5):1734–1738

    Article  CAS  Google Scholar 

  • Prior RL, Cao G (1999) In vivo total antioxidant capacity: comparison of different analytical methods1. Free Radical Biol Med 27(11–12):1173–1181

    Article  CAS  Google Scholar 

  • Samuolienė G, Brazaitytė A, Urbonavičiūtė A, Šabajevienė G, Duchovskis P (2010) The effect of red and blue light component on the growth and development of frigo strawberries. Zemdirbyste-Agriculture 97(2):99–104

    Google Scholar 

  • Sánchez-Sampedro MA, Fernández-Tárrago J, Corchete P (2005) Yeast extract and methyl jasmonate-induced silymarin production in cell cultures of Silybum marianum (L.) Gaertn. J biotechnol 119(1):60–69

    Article  PubMed  CAS  Google Scholar 

  • Shah M, Ullah MA, Drouet S, Younas M, Tungmunnithum D, Giglioli-Guivarc’h N, Hano C, Abbasi BH (2019) Interactive Effects of Light and Melatonin on Biosynthesis of Silymarin and Anti-Inflammatory Potential in Callus Cultures of Silybum marianum (L.) Gaertn. Molecules 24(7):1207

    Article  PubMed Central  CAS  Google Scholar 

  • Shiga T, Shoji K, Shimada H, Hashida S-n, Goto F, Yoshihara T (2009) Effect of light quality on rosmarinic acid content and antioxidant activity of sweet basil Ocimum Basilicum L. Plant Biotechnol 26(2):255–259

    Article  CAS  Google Scholar 

  • Simic SG, Tusevski O, Maury S, Hano C, Delaunay A, Chabbert B, Lamblin F, Lainé E, Joseph C, Hagege D (2015) Fungal elicitor-mediated enhancement in phenylpropanoid and naphtodianthrone contents of Hypericum perforatum L. cell cultures. Plant Cell Tiss Organ Cult 122(1):213–226

    Article  CAS  Google Scholar 

  • Simon JE, Morales MR, Phippen WB, Vieira RF, Hao Z (1999) Basil: a source of aroma compounds and a popular culinary and ornamental herb. Perspect New Crops New Uses 16:499–505

    Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16(3):144–158

  • Sumaryono W, Proksch P, Hartmann T, Nimtz M, Wray V (1991) Induction of rosmarinic acid accumulation in cell suspension cultures of Orthosiphon aristatus after treatment with yeast extract. Phytochemistry 30(10):3267–3271

    Article  CAS  Google Scholar 

  • Tan J, Bednarek P, Liu J, Schneider B, Svatoš A, Hahlbrock K (2004) Universally occurring phenylpropanoid and species-specific indolic metabolites in infected and uninfected Arabidopsis thaliana roots and leaves. Phytochemistry 65(6):691–699

    Article  CAS  PubMed  Google Scholar 

  • Tsuruga A, Terasaka K, Kamiya K, Satake T, Mizukami H (2006) Elicitor-induced activity of isorinic acid 3′-hydroxylase, an enzyme catalyzing the final step of rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures. Plant Biotechnol 23(3):297–301

    Article  CAS  Google Scholar 

  • Werker E, Putievsky E, Ravid U, Dudai N, Katzir I (1993) Glandular hairs and essential oil in developing leaves of Ocimum basilicum L.(Lamiaceae). Ann Bot 71(1):43–50

    Article  CAS  Google Scholar 

  • Wielanek M, Urbanek H (2006) Enhanced glucotropaeolin production in hairy root cultures of Tropaeolum majus L. by combining elicitation and precursor feeding. Plant cell tiss organ cult 86(2):177–186

    Article  CAS  Google Scholar 

  • Yan Q, Shi M, Ng J, Wu JY (2006) Elicitor-induced rosmarinic acid accumulation and secondary metabolism enzyme activities in Salvia miltiorrhiza hairy roots. Plant Sci 170(4):853–858

    Article  CAS  Google Scholar 

  • Yu T-W, Anderson D (1997) Reactive oxygen species-induced DNA damage and its modification: a chemical investigation. Mutat Res 379(2):201–210

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4):283–333

    Article  CAS  PubMed  Google Scholar 

  • Zhao J-L, Zou L, Zhang C-Q, Li Y-Y, Peng L-X, Xiang D-B, Zhao G (2014) Efficient production of flavonoids in Fagopyrum tataricum hairy root cultures with yeast polysaccharide elicitation and medium renewal process. Pharmacogn Mag 10(39):234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Złotek U, Świeca M (2016) Elicitation effect of Saccharomyces cerevisiae yeast extract on main health-promoting compounds and antioxidant and anti-inflammatory potential of butter lettuce (Lactuca sativa L.). J Sci Food Agric 96(7):2565–2572

    Article  PubMed  CAS  Google Scholar 

  • Złotek U, Szymanowska U, Karaś M, Świeca M (2016) Antioxidative and anti-inflammatory potential of phenolics from purple basil (Ocimum basilicum L.) leaves induced by jasmonic, arachidonic and β-aminobutyric acid elicitation. Int J Food Sci Technol 51(1):163–170

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are thankful to department of Biotechnology, Quaid-i-Azam University, Islamabad for providing facilities and support to carry out this research.

Funding

The authors have not disclosed any funding.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Quaid-I-Azam University, Islamabad, 45320, Pakistan

    Gouhar Zaman, Umar Farooq, Muhammad Naeem Bajwa, Muzamil Shah, Riaz Ahmad, Anisa Andleeb & Bilal Haider Abbasi

  2. Institue of Biochemical Sciences, National Taiwan University, Taipei City, 10617, Taiwan

    Hasnain Jan

  3. Laboratoire de Biologie Des Ligneux Et Des Grandes Cultures (LBLGC), INRA USC1328 Université ď Orléans, 45067, Orléans Cedex2, France

    Samantha Drouet & Christophe Hano

Authors
  1. Gouhar Zaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Umar Farooq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Naeem Bajwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hasnain Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muzamil Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Riaz Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anisa Andleeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Samantha Drouet
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christophe Hano
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bilal Haider Abbasi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GZ: performed experiments, TPC and TFC: activities. UF and NB: assisted GZ: with experiments and other biochemical assays. AA and HJ: performed extraction for HPLC. CH and SD: performed HPLC analysis and interpretation. RA and MS: reviewed the manuscript. BHA: concived the idea, facilitated and supervised the research and reviewed the paper critically.

Corresponding author

Correspondence to Bilal Haider Abbasi.

Ethics declarations

Conflict of interest

The authors proclaim no conflict of interest.

Additional information

Communicated by Ali R. Alan.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 396 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zaman, G., Farooq, U., Bajwa, M.N. et al. Effects of yeast extract on the production of phenylpropanoid metabolites in callus culture of purple basil (Ocimum Basilicum L. var purpurascens) and their in-vitro evaluation for antioxidant potential. Plant Cell Tiss Organ Cult 150, 543–553 (2022). https://doi.org/10.1007/s11240-022-02303-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-022-02303-7

Keywords

Search

Navigation