The Parasitic Plant Cistanche violacea (Desf.) Beck from Ghardaïa (Algeria): A Source of Biologically Active Compounds

Year 2024, Volume: 11 Issue: 2, 433 - 452, 15.05.2024

Nadjette Djemouaı , Somia Saad Faiza Baali Hassina Meguellati Hanane Benzetta Abdelhamid Foughalia

https://doi.org/10.18596/jotcsa.1291696

Abstract

The present study aims to determine the contents of total polyphenol (TPC) and total flavonoid (TFC) and evaluate the antioxidant and antimicrobial activities of Cistanche violacea (Desf.) Beck. The extraction of bioactive compounds from the whole plant of C. violacea (Desf.) Beck was carried out by three different methods, including maceration, Soxhlet, and ultrasound, with ethanol and water as solvents. The results showed that the ultrasound ethanolic extract recorded the greatest amounts of TPC with 188.95 ± 2.2μg gallic acid equivalent/mg dry extract, while for TFC, it was the maceration ethanolic extract with 40.26 ± 6.02µg quercetin equivalent/mg dry extract. The High-Performance Liquid Chromatography (HPLC) results showed the presence of phenolic compounds, with 32 identified compounds in the ethanolic and aqueous extracts. The different extracts showed antioxidant capacities for DPPH, ABTS, phenanthroline, and reducing power assays. The highest antioxidant ability was observed with the ethanolic extract obtained by the maceration method (IC50 33.35 ± 1.4 and IC50 < 12.5 μg/mL for DPPH and ABTS tests). The antimicrobial investigation on seven microbial strains revealed that the ethanolic extract ultrasound showed moderate antibacterial activity (18.66 ± 1.1mm) against only Staphylococcus aureus ATCC25923, while the other extracts showed weak or no antimicrobial activity. This work suggests that C. violacea (Desf.) Beck has antioxidant properties of natural origin, which justify its traditional use in treating many conditions related to oxidative stress.

Keywords

Cistanche violacea, extracts, phenolic compounds, HPLC, antioxidant potential, antimicrobial activity.

Thanks

The authors acknowledge the Ministry of Higher Education and Scientific Research of Algeria (MESRS) and the General Direction of Scientific Research and Technological Development (DGRSDT), the Center for Scientific and Technical Research on Arid Regions (CRSTRA), Biskra, Algeria and the University of Ghardaia, Ghardaïa, Algeria.

References

• 1. Bennett JR, Mathews S. Phylogeny of the parasitic plant family Orobanchaceae inferred from phytochrome A. American Journal of Botany. 2006 Jul;93(7):1039-1051. <URL>.
• 2. Mutuku JM, Cui S, Yoshida S, Shirasu K. Orobanchaceae parasite–host interactions. New Phytologist. 2021 Apr;230(1):46-59. <URL>.
• 3. Heide-Jørgensen HS. Introduction: the parasitic syndrome in higher plants. In: Joel D, Musselman LJ, Gressel J, editors. Parasitic Orobanchaceae. Heidelberg: Springer Berlin; 2013 Jan. P. 1-20. <URL>.
• 4. Piwowarczyk R, Ochmian I, Lachowicz S, Kapusta I, Sotek Z, Błaszak M. Phytochemical parasite-host relations and interactions: A Cistanche armena case study. Science of The Total Environment. 2020 May;716,137071. <URL>.
• 5. Westwood JH, Yoder JI, Timko MP, de Pamphilis CW. The evolution of parasitism in plants. Trends in Plant Science. 2010 Apr;15(4):227-235. <URL>.
• 6. Piwowarczyk R, Sánchez Pedraja Ó, Moreno Moral G, Fayvush G, Zakaryan N, Kartashyan N, Aleksanyan A. Holoparasitic Orobanchaceae (Cistanche, Diphelypaea, Orobanche, Phelipanche) in Armenia: distribution, habitats, host range and taxonomic problems. Phytotaxa. 2019 Jan;386(1):001-106. <URL>.
• 7. Quezel P, Santa S. Nouvelle flore d'Algérie et des régions désertiques méridionales.Tomes 2. Edition CNRS; Paris; 1963. 1170p. ISBN: IF5841. <URL>.
• 8. Hammiche V, Maiza K. Traditional medicine in Central Sahara: Pharmacopoeia of Tassili N’ajjer. Journal of Ethnopharmacology. 2006 May;105:358-367. <URL>.
• 9. Beladjila KA, Berrehal D, De Tommasi N, Granchi C, Bononi G, Braca A, De Leo M. New phenylethanoid glycosides from Cistanche phelypaea and their activity as inhibitors of monoacylglycerol lipase (MAGL). Planta Medica. 2018 Jan;84:710-715. <URL>.
• 10. Bougandoura A, D'Abrosca B, Ameddah S, Scognamiglio M, Mekkiou R, Fiorentino A, Benayache S, Benayache F. Chemical constituents and in vitro anti-inflammatory activity of Cistanche violacea Desf. (Orobanchaceae) extract. Fitoterapia. 2016 Mar;109:248-253. <URL>.
• 11. Alia F, CHouikh A, Djahra AB, Bousbia Brahim A, Nani S, Tliba A. Comparative study of some physicochemical and biological properties of effect host species variation on the relationship Saharan parasitic plant Cistanche violacea (Desf.) Beck. Notulae Scientia Biologicae. 2021 Nov;13(4):11054. <URL>.
• 12. Debouba M, Balti R, Hwiwi S, Zouari S. Antioxidant capacity and total phenols richness of Cistanche violacea hosting Zygophyllum album. International Journal of Phytomedicine. 2012; 4(3):399-402. <URL>.
• 13. Ben Attia I, Zucca P, Marincola FC, Nieddu M, Piras A, Rosa A, Rescigno A, Chaieb M. Evaluation of the antioxidant and cytotoxic activities on cancer cell line of extracts of parasitic plants harvested in Tunisia. Polish Journal of Food and Nutrition Science. 2020 Mar;70(3):253-263. <URL>.
• 14. Bouzayani B, Koubaa I, Frikha D, Samet S, Ben Younes A, Chawech R, Maalej S, Allouche N, Mezghani Jarraya R. Spectrometric analysis, phytoconstituents isolation and evaluation of in vitro antioxidant and antimicrobial activities of Tunisian Cistanche violacea (Desf). Chemical Papers. 2022 Jan;76(5):3031-3050. <URL>.
• 15. Abdallah, EM. Antimicrobial evaluation of flowering stalks of Cistanche violacea, a holoparasitic plant collected from arid region in Qassim, Saudi Arabia. Pharmaceutical and Biological Evaluations. 2017 Dec;4(6):239-244. <URL>.
• 16. Mihoub R, Chabour N, Guermoui M. Modeling soil temperature based on Gaussian process regression in a semi-arid-climate, case study Ghardaia, Algeria. Geomechanics and Geophysics for Geo-Energy and Geo-Resources. 2016 Jul;2:397-403. <URL>.
• 17. Singleton VL, Orthofer R, Lamuela-Raventos RM. Analysis of total phenols and other oxidants substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology. 1999;299:152-178. <URL>.
• 18. Zhishen J, Mengcheng T, Jianming W. Research on antioxidant activity of flavonoids from natural materials. Food Chemistry. 1999 Mar;64:555-559. <URL>.
• 19. Meguellati H, Ouafi S, Saad S, Harchaoui L, Djemouai N. Phytochemical characterization, in vivo and in vitro biological activities of Atriplex lindleyi Moq. subsp. inflata. Journal of Ethnopharmacology. 2024 Jan;117333. <URL>.
• 20. Blois MS. Antioxidant determinations by the use of a stable free radical. Nature. 1958;181(4617):1119-1200. <URL>.
• 21. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine Journal. 1999 May;26(98):1231-1237. <URL>.
• 22. Oyaizu M. Studies on products of browning reaction: Antioxidative activities of products of browning reaction prepared from glucosamine. The Japanese Journal of Nutrition and Dietetics. 1986;44(6):307-315. <URL>.
• 23. Szydlowska-Czerniak A, Dianoczki C, Recseg K, Karlovits G, Szlyk E. Determination of antioxidant capacities of vegetable oils by ferric-ion spectrophotometric methods. Talanta. 2008 Aug;76(4):899-905. <URL>.
• 24. Pérez C, Agnese AM, Cabrera JL. The essential oil of Senecio graveolens (Compositae): Chemical composition and antimicrobial activity tests. Journal of Ethnopharmacology. 1999 Jul;66(1):91-96. <URL>.
• 25. Miliauskas G, Venskutonis PR, Van Beek, TA. Screening of radical scavenging activity of some me-dicinal and aromatic plant extract. Food chemistry. 2004 Apr;85(2):231-237. <URL>.
• 26. Ebrahimi NS, Hadian J, Mirjalili MH, Sonboli A, Yousefzadi M. Essential oil composition and antibacteri-al activity of Thymus caramanicus at different phono-logical stages. Food Chemistry. 2008 Oct;110(4):927-931. <URL>.
• 27. Nićiforović N, Abramovič H. Sinapic acid and its derivatives: Natural sources and bioactivity. Compre-hensive Reviews in Food Science and Food Safety. 2014 Jan;13(1):34-51. <URL>.
• 28. Sharma A, Sidhu GP, Araniti F, Bali AS, Shahzad B, Tripathi DK, Brestic M, Skalicky M, Landi M. The role of salicylic acid in plants exposed to heavy metals. Mole-cules. 2020 Jan;25(3):540. <URL>.
• 29. Njus D, Kelley PM, Tu Y, Schlegel HB. Ascorbic acid: The chemistry underlying its antioxidant proper-ties. Free Radical Biology and Medicine. 2020 Nov;159:37-43. <URL>.
• 30. Küpeli Akkol E, Genç Y, Karpuz B, Sobarzo-Sánchez E, Capasso R. Coumarins and coumarin-related compounds in pharmacotherapy of cancer. Cancers. 2020 Jul;12(7):1959. <URL>.
• 31. Bai J, Zhang Y, Tang C, Hou Y, Ai X, Chen X, Zhang Y, Wang X, Meng X. Gallic acid: Pharmacological activi-ties and molecular mechanisms involved in inflamma-tion-related diseases. Biomedicine & Pharmacotherapy. 2021 Jan;133:110985. <URL>.
• 32. Purba R, Paengkoum S, Paengkoum P. Develop-ment of a simple high-performance liquid chromatog-raphy-based method to quantify synergistic compounds and their composition in dried leaf extracts of Piper sarmentosum Roxb. Separations. 2021 Sep;8(9):152. <URL>.
• 33. Singab RA, Elleboudy NS, Elkhatib WF, Yassein MA, Hassouna NA. Improvement of caffeic acid biotrans-formation into para‐hydroxybenzoic acid by Candida albicans CI‐24 via gamma irradiation and model‐based optimization. Biotechnology and Applied Biochemistry. 2021 Apr;69(2):469-478. <URL>.
• 34. Olatunde A, Mohammed A, Ibrahim MA, Tajuddeen N, Shuaibu MN. Vanillin: A food additive with multiple biological activities. European Journal of Medicinal Chemistry Reports. 2022 Aug;5: 100055. <URL>.
• 35. Xiao T, Yang L, Chen P, Duan X. Pa-ra hydroxybenzaldehyde against transient focal cere-bral ischemia in rats via mitochondrial preservation. Experimental and Therapeutic Medicine. 2022 Oct;24(6):716. <URL>.
• 36. Li Y, Kong D, Fu Y, Sussman M R, Wu H. The effect of developmental and environmental factors on sec-ondary metabolites in medicinal plants. Plant Physiolo-gy and Biochemistry. 2020 Mar;148:80-89. <URL>.
• 37. Deyama T, Kobayashi(Late) H, Nishibe S, Tu P. Isolation, structure elucidation and Bioactivities of phe-nylethanoid glycosides from Cistanche, Forsythia and Plantago plants. Studies in Natural Products Chemistry. 2006 Mar;33:645-674. <URL>.
• 38. Rahim, Meriem Z., Bhakti Prinsi, Luca Espen, Tarek Benabdelkader, Mohamed Nabiev, and Karim Houali. Comparative analysis of the chemical constituents and in vitro antioxidant activities of different aqueous extracts of Cistanche phelypaea (L.) Cout. from Algeria. South African Journal of Botany. 2022 August;148:259-267. <URL>.
• 39. Kabtni S, Sdouga D, Bettaib Rebey I, Save M, Trifi-Farah N, Fauconnier ML, Marghali S. Influence of climate variation on phenolic composition and antioxidant capacity of Medicago minima populations. Scientific reports. 2020 May;10(1):1-15. <URL>.
• 40. Aboul-Enein AM, El-Ela FA, Shalaby EA, El-Shemy HA. Traditional medicinal plants research in Egypt: Studies of antioxidant and anticancer activities. Journal of Medicinal Plant Research. 2012 Feb;6(5):689-703. <URL>.
• 41. Trampetti F, Pereira C, Rodrigues MJ, Celaj O, D’Abrosca B, Zengin G, Mollica A, Stefanucci A, Custódio L. Exploring the halophyte Cistanche phelypaea (L.) Cout as a source of health promoting products: In vitro antioxidant and enzyme inhibitory properties, metabolomic profile and computational studies. Journal of Pharmaceutical and Biomedical Analysis. 2019 Feb;165:119-128. <URL>.
• 42. Wang X, Wang J, Guan H, Xu R, Luo X, Su M, Chang X, Tan W, Chen J, Shi Y. Comparison of the chemical profiles and antioxidant activities of different parts of cultivated Cistanche deserticola using ultra performance liquid chromatography-quadrupole time-of-flight mass spectrometry and a 1, 1-diphenyl-2-picrylhydrazyl-based assay. Molecules. 2017 Nov;22(11):2011. <URL>.
• 43. Hamed SEM, EL-Kamali HH. Antibacterial properties of methanolic and aqueous extracts of some plants against some Enterobacteriaceae species. Open Access Library Journal. 2016 Mar;3:e2488. <URL>.
• 44. Keymanesh K, Hamedi J, Moradi S, Mohammadipanah F, Sardari S. Antibacterial and antifungal and toxicity of rare Iranian plants. International Journal Pharmacology. 2009;5(1):81-85. <URL>.
• 45. Ullah N, Rehman A, Ahmad S, Samad N, Andaleeb H, Ahmad W, Ahmad K, Haroon M, Maqbool S, Altaf A, Raza N. Antimicrobial assay and minimum inhibitory concentration values of Cistanche tubulosa. International Journal of Current Microbiology and Applied Sciences. 2016 Feb;5(2):380-388. <URL>.
• 46. Adnan M, Bibi R, Mussarat S, Tariq A, Shinwari ZK. Ethnomedicinal and phytochemical review of Pakistani medicinal plants used as antibacterial agents against Escherichia coli. Annals of Clinical Microbiology and Antimicrobials. 2014 Aug;13(1):40. <URL>.
• 47. Fidrianny I, Rizkiya A, Ruslan K. Antioxidant activities of various fruit extracts from three Solanum sp. using DPPH and ABTS method and correlation with phenolic, flavonoid and carotenoid content. Journal of Chemical and Pharmaceutical Research. 2015 Jan;7(5):666-672. <URL>.
• 48. Ali A, Shahu R, Balyan P, Kumari S, Ghodmare R, Jobby R, Jha P. Antioxidation and antiglycation properties of a natural sweetener: Stevia rebaudiana. Sugar Tech. 2022 Mar-Apr; 24(2):563–575. <URL>.
• 49. Wang C, Cheng D, Cao J, Jiang W. Antioxidant capacity and chemical constituents of Chinese jujube (Ziziphus jujuba Mill.) at different ripening stages. Food Science and Biotechnology. 2013 Jun;22(3):639-644. <URL>.
• 50. Pourmorad F, Hosseinimehr S J, Shahabimajd N. Antioxidant activity, phenol and flavonoid contents of some selected Iranian medicinal plants. African Journal of Biotechnology. 2006 Jun;5(11): 1142-1145. <URL>.
• 51. Kalia K, Sharma K, Singh HP, Singh B. Effects of extraction methods on phenolic contents and antioxidant activity in aerial parts of Potentilla atrosanguinea Lodd. and quantification of its phenolic constituents by RP-HPLC. Journal of Agricultural and Food Chemistry. 2008 Oct;56(21):10129-10134. <URL>.
• 52. Amri O, Elguiche R, Tahrouch S, Zekhnini A, Hatimi A. Antifungal and antioxidant activities of some aromatic and medicinal plants from the southwest of Morocco. Journal of Chemical and Pharmaceutical Research. 2015 Jul;7(7):672-678. <URL>.