Farm or Lab? A Comparative Study of Oregano’s Leaf and Callus Volatile Isolates Chemistry and Cytotoxicity

Oregano (Origanum vulgare, Lamiaceae plant family) is a well-known aromatic herb with great commercial value, thoroughly utilized by food and pharmaceutical industries. The present work regards the comparative assessment of in vitro propagated and commercially available oregano tissue natural products. This study includes their secondary metabolites’ biosynthesis, antioxidant properties, and anticancer activities. The optimization of callus induction from derived oregano leaf explants and excessive oxidative browning was performed using various plant growth regulators, light conditions, and antioxidant compounds. The determination of oregano callus volatiles against the respective molecules in maternal herbal material was performed using gas chromatography–mass spectrometry (GC/MS) analysis. In total, the presence of twenty-seven phytochemicals was revealed in both leaf and callus extracts, from which thirteen molecules were biosynthesized in both tissues studied, seven compounds were present only in callus extracts, and seven metabolites only in leaf extracts. Carvacrol and sabinene hydrate were the prevailing volatiles in all tissues exploited, along with alkanes octacosane and triacontane and the trimethylsilyl (TMS) derivative of carvacrol that were detected in significant amounts only in callus extracts. The MTT assay was employed to assess the in vitro cytotoxic properties of oregano extracts against the epithelial human breast cancer MDA-MB-231 and the human neuroblastoma SK-N-SH cell lines. The extracts displayed concentration and time-dependent responses in cell proliferation rates.

[1]  F. Maggi,et al.  Natural diversity in phenolic components and antioxidant properties of oregano (Origanum vulgare L.) accessions, grown under the same conditions , 2022, Scientific Reports.

[2]  Sangdun Choi,et al.  Role of Plant-Derived Active Constituents in Cancer Treatment and Their Mechanisms of Action , 2022, Cells.

[3]  Y. Shukla,et al.  Phyto-factories of anti-cancer compounds: a tissue culture perspective , 2022, Beni-Suef University Journal of Basic and Applied Sciences.

[4]  S. Jahan,et al.  Plants in Anticancer Drug Discovery: From Molecular Mechanism to Chemoprevention , 2022, BioMed research international.

[5]  Chunxiang Yang,et al.  Evaluation of the slow-release polylactic acid/polyhydroxyalkanoates active film containing oregano essential oil on the quality and flavor of chilled pufferfish (Takifugu obscurus) fillets. , 2022, Food chemistry.

[6]  Vijay Kumar Chattu,et al.  Cancer Incidence, Mortality, Years of Life Lost, Years Lived With Disability, and Disability-Adjusted Life Years for 29 Cancer Groups From 2010 to 2019 , 2021, JAMA oncology.

[7]  M. Niazian,et al.  Traditional in vitro strategies for sustainable production of bioactive compounds and manipulation of metabolomic profile in medicinal, aromatic and ornamental plants , 2021, Planta.

[8]  Tanja M Lunić,et al.  The Marvellous Oregano Spices , 2021, Foods 2021.

[9]  Xiaodong Wang,et al.  UPLC–MS-Based Non-targeted Analysis of Endogenous Metabolite Changes in the Leaves of Scabiosa tschiliensis Grüning Induced by 6-Benzylaminopurine and Kinetin , 2021, Frontiers in Plant Science.

[10]  M. Serafini,et al.  Antitumor Effects of Carvacrol and Thymol: A Systematic Review , 2021, Frontiers in Pharmacology.

[11]  Yuan K. Liu,et al.  Development of Origanum vulgare Cell Suspension Culture to Produce Polyphenols and the Stimulation Effect of Salicylic Acid Elicitation and Phenylalanine Feeding , 2021, Biotechnology and Bioprocess Engineering.

[12]  G. Zengin,et al.  Health beneficial and pharmacological properties of p-cymene. , 2021, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[13]  L. Almagro,et al.  Improved biotechnological production of paclitaxel in Taxus media cell cultures by the combined action of coronatine and calix[8]arenes. , 2021, Plant physiology and biochemistry : PPB.

[14]  I. Dubery,et al.  Application of Plant Growth Regulators Modulates the Profile of Chlorogenic Acids in Cultured Bidens pilosa Cells , 2021, Plants.

[15]  M. Nadeem,et al.  UV-C mediated accumulation of pharmacologically significant phytochemicals under light regimes in in vitro culture of Fagonia indica (L.) , 2021, Scientific reports.

[16]  A. Jemal,et al.  Cancer Statistics, 2021 , 2021, CA: a cancer journal for clinicians.

[17]  I. D. Cavalcanti,et al.  Advances in Cancer Treatment: From Systemic Chemotherapy to Targeted Therapy , 2021 .

[18]  J. Boutin,et al.  Secure and Sustainable Sourcing of Plant Tissues for the Exhaustive Exploration of Their Chemodiversity , 2020, Molecules.

[19]  S. Haroutounian,et al.  Farm or lab? Chamazulene content of Artemisia arborescens (Vill.) L. essential oil and callus volatile metabolites isolate , 2020 .

[20]  Seyed Mousa Mousavi Kouhi,et al.  Optimization of Callus Induction with Enhancing Production of Phenolic Compounds Production and Antioxidants Activity in Callus Cultures of Nepeta binaloudensis Jamzad (Lamiaceae) , 2020, Iranian journal of biotechnology.

[21]  S. Haroutounian,et al.  Volatile systematics: A novel biochemical interpretation of essential oil compounds enhances their chemophenetic significance , 2020 .

[22]  J. Miao,et al.  Recent Advances in the Tissue Culture of American Ginseng (Panax quinquefolius) , 2020, Chemistry & biodiversity.

[23]  J. Vizmanos,et al.  Improvement of antioxidant activity of oregano (Origanum vulgare L.) with an oral pharmaceutical form. , 2020, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[24]  Hema Chandran,et al.  Plant tissue culture as a perpetual source for production of industrially important bioactive compounds , 2020, Biotechnology reports.

[25]  Byoung Ryong Jeong,et al.  Callus induction and browning suppression in tree peony Paeonia ostii ‘Fengdan’ , 2020, Horticulture, Environment, and Biotechnology.

[26]  Pierre Ducrot,et al.  Unraveling Plant Natural Chemical Diversity for Drug Discovery Purposes , 2020, Frontiers in Pharmacology.

[27]  Z. Yordanova,et al.  Green (cell) factories for advanced production of plant secondary metabolites , 2020, Critical reviews in biotechnology.

[28]  Oleynikov Vladislav Antioxidant and antimicrobial properties of oregano extract (Origani vulgaris herba L.) , 2020 .

[29]  E. Nishihara,et al.  Exogenous Kinetin Promotes the Nonenzymatic Antioxidant System and Photosynthetic Activity of Coffee (Coffea arabica L.) Plants Under Cold Stress Conditions , 2020, Plants.

[30]  C. Dall’Aglio,et al.  Oregano Feed Supplementation Affects Glycoconjugates Production in Swine Gut , 2020, Animals : an open access journal from MDPI.

[31]  S. Sen,et al.  Herbal Medicine in India: Indigenous Knowledge, Practice, Innovation and its Value , 2020 .

[32]  P. Ranjekar,et al.  Phytochemicals in Cancer Treatment: From Preclinical Studies to Clinical Practice , 2020, Frontiers in Pharmacology.

[33]  G. Kaltsas,et al.  Bioelectrical Analysis of Various Cancer Cell Types Immobilized in 3D Matrix and Cultured in 3D-Printed Well , 2019, Biosensors.

[34]  S. Kintzios,et al.  Anticancer and biochemical effects of Viscum album L. protein extracts on HeLa cells , 2019, Plant Cell, Tissue and Organ Culture (PCTOC).

[35]  E. Heidarian,et al.  Antiproliferative and Anti-invasion Effects of Carvacrol on PC3 Human Prostate Cancer Cells through Reducing pSTAT3, pAKT, and pERK1/2 Signaling Proteins , 2019, International journal of preventive medicine.

[36]  S. Srivastava,et al.  Role of Phytochemicals in Cancer Prevention , 2019, International journal of molecular sciences.

[37]  M. Adil,et al.  Red light controlled callus morphogenetic patterns and secondary metabolites production in Withania somnifera L. , 2019, Biotechnology reports.

[38]  N. Krigas,et al.  In vitro propagation of medicinal and aromatic plants: the case of selected Greek species with conservation priority , 2019, In Vitro Cellular & Developmental Biology - Plant.

[39]  E. Skoufogianni,et al.  Ecology, Cultivation and Utilization of the Aromatic Greek Oregano (Origanum vulgare L.): A Review , 2019, Notulae Botanicae Horti Agrobotanici Cluj-Napoca.

[40]  Q. Peng,et al.  Simultaneous defeat of MCF7 and MDA-MB-231 resistances by a hypericin PDT–tamoxifen hybrid therapy , 2019, npj Breast Cancer.

[41]  Jacob P Veenstra,et al.  Oregano (Origanum vulgare) extract for food preservation and improvement in gastrointestinal health. , 2019, International journal of nutrition.

[42]  T. Efferth Biotechnology Applications of Plant Callus Cultures , 2019, Engineering.

[43]  M. Arif,et al.  Silver nanoparticles elicited in vitro callus cultures for accumulation of biomass and secondary metabolites in Caralluma tuberculata , 2019, Artificial cells, nanomedicine, and biotechnology.

[44]  A. Chattopadhyay,et al.  Cultivation of Medicinal Plants: Special Reference to Important Medicinal Plants of India , 2019, Herbal Medicine in India.

[45]  Alexandra Husičková,et al.  Role of Cytokinins in Senescence, Antioxidant Defence and Photosynthesis , 2018, International journal of molecular sciences.

[46]  R. Bellini,et al.  From Bio-Prospecting to Field Assessment: The Case of Carvacrol Rich Essential Oil as a Potent Mosquito Larvicidal and Repellent Agent , 2018, Front. Ecol. Evol..

[47]  Massimo Libra,et al.  Evolution of Cancer Pharmacological Treatments at the Turn of the Third Millennium , 2018, Front. Pharmacol..

[48]  A. Siddique,et al.  Effect of light and dark on callus induction and regeneration in tobacco (Nicotiana tabacum L.) , 2018, Bangladesh Journal of Botany.

[49]  P. Ahmad,et al.  Potential of exogenously sourced kinetin in protecting Solanum lycopersicum from NaCl-induced oxidative stress through up-regulation of the antioxidant system, ascorbate-glutathione cycle and glyoxalase system , 2018, PloS one.

[50]  V. Nazeri,et al.  Essential oil profile of oregano (Origanum vulgare L.) populations grown under similar soil and climate conditions , 2018, Industrial Crops and Products.

[51]  M. R. D. S. Vieira,et al.  Physiological Effect of Kinetin on the Photosynthetic Apparatus and Antioxidant Enzymes Activities During Production of Anthurium , 2018, Horticultural Plant Journal.

[52]  L. Chuang,et al.  Ethanolic Extract of Origanum vulgare Suppresses Propionibacterium acnes-Induced Inflammatory Responses in Human Monocyte and Mouse Ear Edema Models , 2018, Molecules.

[53]  G. Buchbauer,et al.  α-Terpineol, a natural monoterpene: A review of its biological properties , 2018 .

[54]  Fereshteh Bagheri,et al.  Shikonin Production by Callus Culture of Onosma bulbotrichom as Active Pharmaceutical Ingredient , 2018, Iranian journal of pharmaceutical research : IJPR.

[55]  J. Heredia,et al.  Flavonoids and Phenolic Acids from Oregano: Occurrence, Biological Activity and Health Benefits , 2017, Plants.

[56]  D. P. de Sousa,et al.  Analgesic-Like Activity of Essential Oil Constituents: An Update , 2017, International journal of molecular sciences.

[57]  Shunsuke Watanabe,et al.  Wounding Triggers Callus Formation via Dynamic Hormonal and Transcriptional Changes1[OPEN] , 2017, Plant Physiology.

[58]  A. Alarcon‐Rojo,et al.  Oregano Essential Oil in Animal Production , 2017 .

[59]  Tory L. Parker,et al.  Anti-inflammatory, tissue remodeling, immunomodulatory, and anticancer activities of oregano (Origanum vulgare) essential oil in a human skin disease model , 2017, Biochimie open.

[60]  Jianping Chen,et al.  Characterization and Comparative Expression Profiling of Browning Response in Medinilla formosana after Cutting , 2016, Front. Plant Sci..

[61]  G. Bayarmaa,et al.  In vitro Seed Germination and Callus Induction of Ferula ferulaeoides (Steud.) Korov. (Apiaceae) , 2016 .

[62]  W. Yusoff,et al.  Impact of exogenous ascorbic acid on biochemical activities of rice callus treated with salt stress , 2016 .

[63]  A. Steinmetz,et al.  Conservation and sustainable use of medicinal plants: problems, progress, and prospects , 2016, Chinese Medicine.

[64]  Z. Suntres,et al.  Antioxidant, Antibacterial, and Cytotoxic Activities of the Ethanolic Origanum vulgare Extract and Its Major Constituents , 2016, Oxidative medicine and cellular longevity.

[65]  Yonggang Cao,et al.  Carvacrol inhibits proliferation and induces apoptosis in human colon cancer cells , 2015, Anti-cancer drugs.

[66]  A. Castro,et al.  In vitro germination, callus induction and phenolic compounds contents from Pyrostegia venusta (Ker Gawl.) Miers , 2015 .

[67]  Saurabh Bhatia,et al.  Modern Applications of Plant Biotechnology in Pharmaceutical Sciences , 2015 .

[68]  R. Murshed,et al.  Production of tropan alkaloids in the in vitro and callus cultures of Hyoscyamus aureus and their genetic stability assessment using ISSR markers , 2014, Physiology and Molecular Biology of Plants.

[69]  Jiao-Jiao Xu,et al.  Phenolic compounds from Origanum vulgare and their antioxidant and antiviral activities. , 2014, Food chemistry.

[70]  L. Travassos,et al.  Pyrostegia venusta heptane extract containing saturated aliphatic hydrocarbons induces apoptosis on B16F10-Nex2 melanoma cells and displays antitumor activity in vivo , 2014, Pharmacognosy magazine.

[71]  P. Tarantilis,et al.  An assessment of the behavior of carvacrol – rich wild Lamiaceae species from the eastern Aegean under cultivation in two different environments , 2014 .

[72]  Xiuxin Deng,et al.  Comprehensive insights on how 2,4-dichlorophenoxyacetic acid retards senescence in post-harvest citrus fruits using transcriptomic and proteomic approaches , 2013, Journal of experimental botany.

[73]  A. Jones,et al.  Inhibition of Phenylpropanoid Biosynthesis in Artemisia annua L.: A Novel Approach to Reduce Oxidative Browning in Plant Tissue Culture , 2013, PloS one.

[74]  K. Sugimoto,et al.  Plant Callus: Mechanisms of Induction and Repression[OPEN] , 2013, Plant Cell.

[75]  F. Ruiz-Espinoza,et al.  Physiological, morphometric characteristics and yield of Origanum vulgare L. and Thymus vulgaris L. exposed to open-field and shade-enclosure , 2013 .

[76]  L. B. Rangel,et al.  Conventional Cancer Treatment , 2013 .

[77]  D. Leelavathi,et al.  CALLUS INDUCTION AND REGENERATION OF MULTIPLE SHOOTS FROM IN VITRO APICAL BUD EXPLANT OF ORIGANUM VULGARE. AN IMPORTANT MEDICINAL PLANT , 2013 .

[78]  S. R. Bhalsing,et al.  Isolation and characterization of diosgenin from in vitro cultured tissues of Helicteres isora L , 2013, Physiology and Molecular Biology of Plants.

[79]  Xudong Zheng,et al.  Chemical composition, antimicrobial, antioxidant and cytotoxic activity of the essential oil from the leaves of Acanthopanax leucorrhizus (Oliv.) Harms. , 2012, Environmental toxicology and pharmacology.

[80]  Hrudayanath Thatoi,et al.  Biotechnology and Pharmacological Evaluation of Medicinal Plants: An Overview , 2011 .

[81]  H. Naderi-manesh,et al.  Effect of Antioxidants and Carbohydrates in Callus Cultures of Taxus brevifolia: Evaluation of Browning, Callus Growth, Total Phenolics and Paclitaxel Production. , 2011, BioImpacts : BI.

[82]  N. Manzoor,et al.  Cytotoxic effect of Carvacrol on human cervical cancer cells , 2011 .

[83]  A. Kita,et al.  The effect of kinetin on the chlorophyll pigments content in leaves of Zea mays L. seedlings and accumulation of some metal ions , 2011 .

[84]  V. Pence Evaluating costs for the in vitro propagation and preservation of endangered plants , 2011, In Vitro Cellular & Developmental Biology - Plant.

[85]  R. Shibli,et al.  Callusing, Cell Suspension Culture and Secondary Metabolites Production in Persian Oregano (Origanum vulgare L. ) and Arabian Oregano (O. syriacum L.) , 2010 .

[86]  M. P. Guerra,et al.  Enzymatic Browning, Polyphenol Oxidase Activity, and Polyphenols in Four Apple Cultivars: Dynamics during Fruit Development , 2010 .

[87]  F. Afifi,et al.  Volatile oil composition and antiproliferative activity of Laurus nobilis, Origanum syriacum, Origanum vulgare, and Salvia triloba against human breast adenocarcinoma cells. , 2010, Nutrition research.

[88]  E. Gunes,et al.  Analysis of effective factors on information sources at Turkish Oregano farms. , 2010 .

[89]  V. Lattanzio,et al.  Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress , 2009 .

[90]  C. Jayabaskaran,et al.  Enhanced catharanthine and vindoline production in suspension cultures of Catharanthus roseus by ultraviolet-B light , 2008, Journal of molecular signaling.

[91]  S. Kintzios Secondary Metabolite Production from Plant Cell Cultures: the Success Stories of Rosmarinic Acid and Taxol , 2008 .

[92]  K. G. Ramawat,et al.  Bioactive molecules and medicinal plants , 2008 .

[93]  Michal Sharon,et al.  Mechanism of auxin perception by the TIR1 ubiquitin ligase , 2007, Nature.

[94]  R. P. Adams Identification of Essential Oil Components By Gas Chromatography/Mass Spectrometry , 2007 .

[95]  M. Kamalinejad,et al.  Comparison of the Free Radical Scavenging Activity of Six Iranian Achillea. Species , 2006 .

[96]  A. Kamel,et al.  In vivo and in vitro comparative studies of Origanum species , 2006 .

[97]  Peter Nick,et al.  Auxin-Dependent Cell Division and Cell Elongation. 1-Naphthaleneacetic Acid and 2,4-Dichlorophenoxyacetic Acid Activate Different Pathways1 , 2005, Plant Physiology.

[98]  F. Şahin,et al.  In vitro antioxidant, antimicrobial, and antiviral activities of the essential oil and various extracts from herbal parts and callus cultures of Origanum acutidens. , 2004, Journal of agricultural and food chemistry.

[99]  P. Saradhi,et al.  Regeneration of plants from callus cultures of Origanum vulgare L. , 1992, Plant Cell Reports.

[100]  S. Kintzios,et al.  Effect of Medium Composition and Explant Source on the Distribution Profiles Selected Micronutrients in Mistletoe Tissue Cultures , 2003 .

[101]  S. Kintzios,et al.  The Effects of Light on Callus Growth and Somatic Embryogenesis from Lavandula vera and Teucrium chamaedrys: A Preliminary Study , 2002 .

[102]  T. Moritz,et al.  Chapter 2 – Physico-chemical methods of plant hormone analysis , 1999 .

[103]  O. David Sparkman,et al.  Identification of essential oil components by gas chromatography / mass spectroscopy Robert P. Adams , 1997 .

[104]  A. Stomp,et al.  Effects of medium components and light on callus induction, growth, and frond regeneration in Lemna gibba (Duckweed) , 1997, In Vitro Cellular & Developmental Biology - Plant.

[105]  R. Dhindsa,et al.  Leaf senescence and lipid peroxidation: Effects of some phytohormones, and scavengers of free radicals and singlet oxygen , 1982 .

[106]  W. Perman,et al.  Correlation of cocarcinogenic activity among n-alkanes with their physical effects on phospholipid micelles. , 1976, Journal of the National Cancer Institute.

[107]  Y. Masada Analysis of essential oils by gas chromatography and mass spectrometry , 1976 .

[108]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .