Biochemical profile and in vitro biological activities of extracts from seven folk medicinal plants growing wild in southern Tunisia

Autoři: Hajer Tlili aff001;  Najjaa Hanen aff001;  Abdelkerim Ben Arfa aff001;  Mohamed Neffati aff001;  Abdelbasset Boubakri aff001;  Daniela Buonocore aff002;  Maurizia Dossena aff002;  Manuela Verri aff002;  Enrico Doria aff002
Působiště autorů: Laboratory of Pastoral Ecosystems and Valorisation of Spontaneous Plants and Microorganisms, Institute of Arid Regions (IRA), Medenine, Tunisia aff001;  Department of Biology and Biotechnology, University of Pavia, Pavia, Italy aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0213049


Recently, much attention has been paid to the extracts obtained from plant species in order to analyse their biological activities. Due to the climate diversity in Tunisia, the traditional pharmacopoeia consists of a wide arsenal of medicinal plant species since long used in folk medicine, in foods as spices, and in aromatherapy. Although many of these species are nearly facing extinction, only a small proportion of them have been scientifically studied. Therefore, this study explores the biochemical properties of seven spontaneous plants, which were harvested in the arid Tunisian desert: Marrubium vulgare (L.), Rhus tripartita (Ucria) D.C., Thymelaea hirsute (L.) Endl., Plantago ovata (Forsk.), Herniaria fontanesii (J. Gay.), Ziziphus lotus (L.) and Hyoscyamus albus (L.). Extracts from these plants were found to contain different types of secondary metabolites (polyphenols, flavonoids, condensed tannins, crude saponins, carotenoids and alkaloids) that are involved in important biological activities. The biological activity of the extracts obtained from each Tunisian plant was assessed: first of all, leukaemia and colon cancer cell lines (K-562 and CaCo-2 respectively) were treated with different concentrations of extracts, and then the anti-proliferative activity was observed. The results showed, in particular, how the plant extract from Rhus tripartita significantly inhibits cell proliferation, especially on the K-562 tumour cell line. Subsequently, the anti-inflammatory activity was also assessed, and the results showed that Herniaria fontanesii and Marrubium vulgare possess the highest activity in the group of analysed plants. Finally, the greatest acetylcholinesterase inhibitory effect was exhibited by the extract obtained from Rhus tripartita.

In conclusion, all the Tunisian plants we analysed were shown to contain a remarkable amount of different bio-active compounds, thus confirming their involvement in several biological activities. Rhus tripartita and Ziziphus lotus were shown to be particularly effective in anti-proliferative activity, while Herniaria fontanesii were shown to have the best anti-inflammatory activity.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Plants – Medicinal plants – Flowering plants – Lotus – Biochemistry – Antioxidants – Physical sciences – Chemistry – Chemical compounds – Organic compounds – Acetones – Alcohols – Ethanol – Alkaloids – Phenols – Organic chemistry – People and places – Geographical locations – Africa – Tunisia


1. Doit C, Barre J, Cohen R, Bonacorsi S, Bourrillon A, Bingen E. Bactericidal activity against intermediately cephalosporin resistant Streptococcus pneumoniae in cerebrospinal fluid of children with bacterial meningitis treated with high doses of cefotaxime and vancomycin. Antimicrob. Agents Chemother. 1997; 41: 2050–2052. 9303415

2. Essawi T, Srour M. Screening of some Palestinian medicinal plants for antibacterial activity.J Ethnopharmacol. 2000; 70: 343–349. doi: 10.1016/s0378-8741(99)00187-7 10837997

3. Mehtab P, Ali MM, Mahbbob A, Faheem A, Pedro SPS, Manuela RS. Two new phenolic compounds from Ficus rumphii and their antiproliferative activity. J Nat Prod Res. 2014; 28: 646–652.

4. El-Seedi HR, Burman R, Mansour A, Turki Z, Boulos L, Gullbo, J. The traditional medical uses and cytotoxic activities of sixtyone Egyptian plants: discovery of an active cardiac glycoside from Urginea maritima. J. Ethnopharmacol. 2013; 145: 746–757. doi: 10.1016/j.jep.2012.12.007 23228916

5. Ouelbani R, Bensari S, Mouas TN, and Khelifi D. Ethnobotanical investigations on plants used in folk medicine in the regions of Constantine and Mila (North-East of Algeria). J. Ethnopharmacol. 2016; 194: 196–218. doi: 10.1016/j.jep.2016.08.016 27592312

6. Cordell G. Changing strategies in natural products chemistry. Phytochemistry. 1995; 40: 1585–1612

7. Chevallier A. The encyclopedia of medicinal plants. Dorling Kindersley 1996; London

8. Najjaa H, Arfa A, Ben Máthé Á, & Neffati M. Medicinal and Aromatic Plants of the World–Africa 2017; 3.

9. Kabbaj FZ, Meddah B, Cherrah Y, El M, and Faouzi A. Ethnopharmacological profile of traditional plants used in Morocco by cancer patients as herbal therapeutics. Phytopharmacology. 2012; 2: 243–256

10. Marrif HI, Ali BH, Hassan KM. Some pharmacological studies on Artemisia herba-alba (Asso.) in rabbits and mice. J Ethnopharmacol. 1995; 49(1): 51–55 doi: 10.1016/0378-8741(95)01302-4 8786657

11. Le Floc’h E. Contribution à une étude ethnobotanique de la Flore Tunisienne. Pub. Sci. Tunis. Programme Flore et végétation Tunisiennes.1983

12. Le Houerou HN. La vegetation de la Tunisie steppique (avec references au Maroc, en Algérie et la Libye). Ann Inst Nat Rech Agric Tunisie. 1969; 42; 642p

13. Ziyyat A, Legssyer H, Mekhfi H, Dassouli A, Serhouchni M, Benjelloun W. Phytotherapy of hypertension and diabetes in oriental Morocco. J Ethnopharmacol. 1997; 58: 45–54 doi: 10.1016/s0378-8741(97)00077-9 9324004

14. Nait Mbark AZ, Charouf V, Wray M, Nimtz T. Schopke. “Monodesmosidic saponins from Herniaria hirsuta,” Die Pharmazie, 2000; 55(9): 690–692 11031776

15. Rhiouani H, El-Hilaly J, Israili HZ, Lyoussi B. Acute and sub-chronic toxicity of an aqueous extract of the leaves of Herniaria glabra in rodents J. Ethnopharm. 2008; 118: 378–386. doi: 10.1016/j.jep.2008.05.009

16. Madland E. Extraction, Isolation and Structure Elucidation of Saponins from Herniaria incana. Norwegian University of Science and Technology. 2013

17. Hajipoor K, Sani AM. Antibacterial activity of methanol extract and essential oil of Hyosciamus niger against selected pathogenic bacteria. IJBPAS. 2015;4(6):4016–4026.

18. Harrison AP, Bartels EM. A modern appraisal of ancient Etruscan herbal practices. American Journal of Pharmacology and Toxicology. 2006; 1:26–29.

19. Zaabat N, Hay AE, Michalet S, Darbour N, Bayet C, Skandrani I. Antioxidant and antigeno- toxic properties of compounds isolated from Marrubium deserti de Noe. Food Chem Toxicol. 2011; 49(12): 3328–3335. doi: 10.1016/j.fct.2011.08.026 21924316

20. Essawy SS, Abo-elmatty DM, Ghazy NM & Badr JM. Antioxidant and anti-inflammatory effects of Marrubium alysson extracts in high cholesterol-fed rabbits. Saudi Pharmaceutical Journal 2014; 22(5), 472–482.

21. Schlemper V, Ribas A, Nicolau M, Cechinel Filho V. Antispasmodic effects of hydroalcoholic extract of Marrubium vulgare on isolated tissues. Phytomedicine. 1996; 3:211–6. doi: 10.1016/S0944-7113(96)80038-9 23194972

22. Lodhi S, Vadnere G, Sharma V & Usman M. Marrubium vulgare L.: A review on phytochemical and pharmacological aspects. Journal of Intercultural Ethnopharmacology. 2017; 6(4), 429.

23. Pourmorad F, Hosseinimehr SJ, Shahabimajd N. Antioxidant activity, phenol and flavonoid contents of some selected Iranian medicinal plants, African Journal of Biotechnology. 2006; 5(11): 1142–1145.

24. Souri E, Amin G, Farsam H, Arazandeh B, Tehrani M. Screening of antioxidant activity and phenolic content of 24 medicinal plant extracts, DARU. 2008; 16(2) 83–87.

25. Talukder P, Talapatra S, Ghoshal N, Sen Raychaudhuri S. Antioxidant activity and high-performance liquid chromatographic analysis of phenolic compounds during in vitro callus culture of Plantago ovata Forsk. and effect of exogenous additives on accumulation of phenolic compounds. Journal of the Science of Food and Agriculture. 2016; 96(1): 232–244. doi: 10.1002/jsfa.7086 25640456

26. Haddadian K, Haddadian K & Zahmatkash M. A review of plantago plant. Indian Journal of Traditional Knowledge. 2014; 13(4), 681–685.

27. Wu T, McCallum JL, Wang S, Liu R, Zhu H, Tsao R. Evaluation of antioxidant activities and chemical characterization of staghorn sumac fruit (Rhus hirta L.). Food Chemistry. 2013; 138:1333–1340 doi: 10.1016/j.foodchem.2012.10.086 23411251

28. Giancarlo S, Rosa ML, Nadjafi F, Francesco M. Hypoglycaemic activity of two spices extracts: Rhus coriaria L. and Bunium persicum Boiss. Natural Product Research. 2206; 20: 882–886. doi: 10.1080/14786410500520186 16753927

29. Ben Barka Z, Aouadhi C, Tlili M, Alimi H, Ben Miled H, Ben Rhouma K, et al. Evaluation of the anti-diarrheal activity of the hydromethanolic root extract of Rhus tripartita (Ucria) (Anacardiacae). Biomedicine and Pharmacotherapy. 2016;83:827–834. doi: 10.1016/j.biopha.2016.07.055 27501500

30. El-Salam A & Mohammed I. Phytoconstituents and the study of antioxidant, antimalarial and antimicrobial activities of Rhus tripartita growing in Egypt. Journal of Pharmacognosy and Phytochemistry JPP 2015; 4(2), 276–281.

31. El Amrani F, Rhallab A, Alaoui T, El Badaoui K, Chakir S. Hypoglycaemic effect of T. hirsuta in normal and streptozotocininduced diabetic rats. J. Medit. Plant. Res. 2009; 3: 625–629.

32. Kawano M, Matsuyama K, Miyamae Y, Shinmoto H, Kchouk ME, Morio T et al. Antimelanogenesis effect of Tunisian herb Thymelaea hirsuta extract on B16 murine melanoma cells. Experimental Dermatology. 2007; 1612: 977–984

33. Trigui M, Hsouna A. Ben Tounsi S, Jaoua S. Chemical composition and evaluation of antioxidant and antimicrobial activities of Tunisian Thymelaea hirsuta with special reference to its mode of action. Industrial Crops and Products. 2013;41(1):150–157.

34. Borris RP, Blaskó G, Cordell GA. Ethnopharmacologic and phytochemical studies of the Thymelaeaceae. Journal of Ethnopharmacology. 1988; 24:41–91. doi: 10.1016/0378-8741(88)90138-9 3059068

35. Borgi W, Recio MC, Rı´os JL, Chouchane N. Anti-inflammatory and analgesic activities of flavonoid and saponins fractions from Zizyphus lotus (L.) Lam. South African Journal of Botany. 2004; 74:320–324

36. Adzu B., Amos S., Amizan MB., Gamaniel K., 2003. Evaluation of the anti-diarrheal effects of Zizyphus spina-christi stem bark in rats. Acta Tropica.7, 245–50.

37. Renault JH, Ghedira H, Thepenier P, Lavand C, Zeches-Hanrot M, Le Men-Olivier L, Dammarane saponins from Zizyphus lotus. Phytochemistry. 1997;4:1321–7.

38. Abdoul-Azize S, Bendahmane M, Hichami A, Dramane G, Simonin AM, Benammar C et al. Effects of Ziziphus lotus L. (Desf.) polyphenols on Jurkat cell signaling and proliferation. International Immunopharmacology. 2013; 15(2):364–371. doi: 10.1016/j.intimp.2012.11.013 23219580

39. Cuenod A. Flore analytique et synoptique de la Tunisie: Cryptogames vasculaires, Gymnospermes et monocotylédones. 1954. Imprimerie S.E.F.A.N. Tunisie, 287 pp.

40. Medoua G.M., Egal A.A., Oldewage-Theron W.H., 2009. Nutritional value and antioxidant capacity of lunch meals consumed by elderly people of Sharpeville, South Africa. Food Chemistry. 115, 260–264.

41. Lola-Luz T, Hennequart F, Gaffney M. Effect on yield, total phenolic, total flavonoid and total isothiocyanate content of two broccoli cultivars (Brassica oleraceae var italica) following the application of a commercial brown seaweed extract (Ascophyllum nodosum). Agricultural and Food Science. 2014; 23(1): 28–37.

42. Kurilich A, Juvik J. Quantification of carotenoid and tocopherol antioxi- dants in Zea mays. J Agric Food Chem. 1999; 47:1948–1955. doi: 10.1021/jf981029d 10552476

43. Kaur R, Arora S, Thukral AK. Quantitative and qualitative analysis of saponins in different plant parts of Chlorophytum borivialum. Int J Pharm Bio Sci 2015; 6(1), 826–835.

44. Biradar SR, Rachetti BD. Extraction of Some Secondary Metabolites & Thin Layer Chromatography from Different Parts of Centella Asiatica L. (URB). American Journal of Life Sciences. 2013;1(6):243.

45. Moon JK, Shibamoto T. Antioxidant Assays for Plant and Food Components. J. Agric. Food Chem 2009; 57: 1655–1666. doi: 10.1021/jf803537k 19182948

46. Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as measurement of ‘‘antioxidant power”: the FRAP assay. Anal Biochem. 1996; 239: 70–76. doi: 10.1006/abio.1996.0292 8660627

47. Chao HC, Najjaa H, Villareal MO, Ksouri R, Han J, Neffati M, Isoda H. Arthrophytum scoparium inhibits melanogenesis through the down-regulation of tyrosinase and melanogenic gene expressions in B16 melanoma cells. Experimental Dermatology. 2013; 22: 131–136. doi: 10.1111/exd.12089 23362872

48. Sakat SS. In vitro antioxidant and anti-inflammatory activity of methanol extract of Oxalis corniculata linn. International Journal of Pharmacy and Pharmaceutical Sciences 2010;2(1):82–87.

49. Khadri A, Neffati M, Smiti S, Falè P, Lino ARL, Serralheiro MLM et al. Antioxidant, antiacetylcholinesterase and antimicrobial activities of Cymbopogon schoenanthus L. Spreng (lemon grass) from Tunisia. LWT—Food Science and Technology. 2010;43(2):331–336.

50. Abdoul-Azize S. Potential Benefits of Jujube (Zizyphus Lotus L.) Bioactive Compounds for Nutrition and Health. Journal of Nutrition and Metabolism. 2016.

51. Akrout A, Gonzalez LA, El Jani H, Madrid PC. Antioxidant and antitumor activities of Artemisia campestris and Thymelaea hirsuta from southern Tunisia. Food and Chemical Toxicology. 2011;49(2):342–347. doi: 10.1016/j.fct.2010.11.003 21075159

52. Itidel C, Chokri M, Mohamed B, Yosr Z. Antioxidant activity, total phenolic and flavonoid content variation among Tunisian natural populations of Rhus tripartita (Ucria) Grande and Rhus pentaphylla Desf. Industrial Crops and Products. 2013; 51: 171–177.

53. Alghazeer Hussein El-Saltani, Saleh Nabeel, Al-Najjar Asma, Hebail Fatma1. Antioxidant and antimicrobial properties of five medicinal Libyan plants extracts Rabia. Natural Science. 2012; 4: 324–335.

54. Sung B, Chung HY, Kim ND. Role of Apigenin in Cancer Prevention via the Induction of Apoptosis and Autophagy. Journal of Cancer Prevention. 2016: 21(4), 216–226.

55. Perk AA, Shatynska-mytsyk I, Gerçek YC, Boztas K, Yazgan M, Fayyaz S et al. Rutin mediated targeting of signalling machinery in cancer cells. Cancer Cell International. 2014; 14(1), 1–5. doi: 10.1186/1475-2867-14-1

56. Fan FY, Sang LX, Jiang M, McPhee DJ. Catechins and their therapeutic benefits to inflammatory bowel disease. Molecules. 2017; 22(3).

57. Mamta S, Amita K, Eshita M. Micropropogation and Phytochemical Profile Analysis Of Tissue Culture Grown Plantago Ovata Forsk. Asian J Pharm Clin Res. 2017;10 (4):202–206.

58. Ohtera A, Miyamae Y, Nakai N. Identification of 6-octadecynoic acid from a methanol extract of Marrubium vulgare L. as a peroxisome proliferator-activated receptor gamma agonist. Biochem Biophys Res Commun 2013;440(2):204–209. doi: 10.1016/j.bbrc.2013.09.003 24025677

59. Nargund LV, Redd GR, Hariprasad V. Inhibition of albumin denaturation and anti-inflammatory activity of acetamido [(phenyl-4'-yl)-oxymethyl)]2-(p-substituted phenylamino)-1,2,4-triazoles and -1,3,4-thiadiazoles. Indian J Exp Biol. 1993;31(4):395–6. 8359842

60. Saso L, Valentini G, Casini ML, Grippa E, Gatto MT, Leone MG et al.Inhibition of heat-induced denaturation of albumin by nonsteroidal antiinflammatory Drugs (NSAIDs): pharmacological implications. Arch Pharmacol Res. 2001; 24: 150–158

61. Chatterjee P, Chandra S, Dey P, Bhattacharya S. Evaluation of anti-infammatory effects of green tea and black tea: a comparative in vitro study. J Adv Pharm Technol Res. 2012; 3: 136–138. doi: 10.4103/2231-4040.97298 22837963

62. García-Ayllón M-S, Small DH, Avila J, Sáez-Valero J. Revisiting the Role of Acetylcholinesterase in Alzheimer’s Disease: Cross-Talk with P-tau and β-Amyloid. Frontiers in Molecular Neuroscience. 2011; 4:22. doi: 10.3389/fnmol.2011.00022 21949503

63. Fawole OA, Amoo SO, Ndhlala AR, Light ME, Finnie JF, Van Staden J. Anti-inflammatory, anticholinesterase, antioxidant and phytochemical properties of medicinal plants used for pain-related ailments in South Africa. J. Ethnopharmacol. 2010; 127: 235–241 doi: 10.1016/j.jep.2009.11.015 19932161

64. Hernandez MF, Falé PLV, Araújo MEM, Serralheiro MLM. Acetylcholinesterase inhibition and antioxidant activity of the water extracts of several Hypericum species. Food Chem. 2010; 120: 1076–1082.

65. Orhan IE, Belhattab R, Șenol FS, Gülpİnar AR, Hoșbaș S, Kartal M. Profiling of cholinesterase inhibitory and antioxidant activities of Artemisia absinthium, A. herba-alba, A. fragrans, Marrubium vulgare, M. astranicum, Origanum vulgare subsp. glandulossum and essential oil analysis of two Artemisia species. Industrial Crops and Products. 2010; 32(3): 566–571.

66. Loïzzo MR, Tundis R, Conforti F, Menichini F, Bonesi M, Nadjafi F et al.Salvia leriifolia Benth (Lamiaceae) extract demonstrates in vitro antioxidant properties and cholinesterase inhibitory activity. Nutr. Res. 2010; 30: 823–83. doi: 10.1016/j.nutres.2010.09.016 21147365

67. Adewusi EA, Moodley N, Steenkamp V. Antioxidant and acetylcholinesterase inhibitory activity of selected southern African medicinal plants. S. Afr. J. Bot. 2011; 77:638–644

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