Analysis of the Metabolic Profile and Biological Activity of Hawthorn Species twigs: Crataegus azarolus and Crataegus monogyna

Hiwa Sheikh Ahmed Qalatobzany; Kadhm Abdullah Muhammad; Djshwar Dhahir Lateef; Kamaran Salh Rasul; Abdulrahman Smail Ibrahim; Mariana Casari Parreira; Weria Weisany

doi:10.24017/science.2025.1.8

Authors

Hiwa Sheikh Ahmed Qalatobzany Department of Chemistry, College of Science, University of Garmian, Kalar, Sulaymaniyah, Iraq https://orcid.org/0000-0003-1144-9295
Kadhm Abdullah Muhammad Department of Agribusiness and Rural Development, College of Agricultural Engineering Sciences, Universi-ty of Sulaimani, Sulaymaniyah, Iraq
Djshwar Dhahir Lateef Department of Biotechnology and Crop Sciences, College of Agricultural Engineering Sciences, University of Sulaimani, Sulaymaniyah, Iraq https://orcid.org/0000-0001-7005-6630
Kamaran Salh Rasul Department of Horticulture, College of Agricultural Engineering Sciences, University of Sulaimani, Sulaymaniyah, Iraq https://orcid.org/0000-0002-5640-4982
Abdulrahman Smail Ibrahim School of Agrarian and Environmental Sciences, University of Azores, Terceira Island, Portugal https://orcid.org/0000-0002-0714-6585
Mariana Casari Parreira School of Agrarian and Environmental Sciences, University of Azores, Terceira Island, Portugal
Weria Weisany Department of Agriculture and Food Science, Science and Research Branch, Islamic Azad University, Tehran, Iran https://orcid.org/0000-0002-0260-0902

Abstract

All parts of the hawthorn tree (Crataegus spp.), including fruits, flowers, and leaves, have been used as a source of bioactive compounds. Thus, in this investigation, the twigs of two species of hawthorn plant of Crataegus azarolus (C. azarolus) and Crataegus monogyna (C. monogyna) were evaluated for bioactive compositions and biological activity (antioxidant and antimicrobial activities). To evaluate bioactive compositions, high-performance liquid chromatography (HPLC) was applied, and for biological activity, biochemical assays were performed. C. monogyna revealed a higher amount of total phenolic, total flavonoid, and total tannin contents compared to C. azarolus. The HPLC results indicated the highest amount of kaempferol (14.40%), catechin (17.70%), and gallic acid (25%) in twigs of C. azarolus, while the maximum quercetin (72%) compound was present in C. monogyna. C. monogyna exhibited higher antioxidant activity by 1,1-dizarophenyl-2-picrylhydrazyl (DPPH) (86.13%) and 2,2′-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid (ABTS) (92.93%) compared to C. azarolus for antioxidant activity-DPPH (81.86%) and -ABTS (87.47%) assay. In the case of antimicrobial activity, the twigs of both species (especially C. azarolus) have a capacity against Bacillus subtilis, Staphylococcus aureus, and methicillin-resistant Staphylococcus aureus. The results of this study revealed that the twigs of both species contained a high amount of phenolic metabolites and antioxidant activity, while they showed low antimicrobial activity.

Keywords:

Crataegus species, Chemical composition, Secondary metabolite, Antioxidant activity, Antimicrobial activity

References

K. O. Radha and N. R. Khwarahm, “An Integrated Approach to Map the Impact of Climate Change on the Distri-butions of Crataegus azarolus and Crataegus monogyna in Kurdistan Region, Iraq,” Sustainability, vol. 14, no. 21, 2022, doi: 10.3390/su142114621.

J. Zhang, X. Chai, F. Zhao, G. Hou, and Q. Meng, “Food Applications and Potential Health Benefits of Hawthorn,” Foods, vol. 11, no. 18, 2022, doi: 10.3390/foods11182861.

A. Nazhand et al., “Hawthorn (Crataegus spp.): An Updated Overview on Its Beneficial Properties,” Forests, vol. 11, no. 5, 2020, doi: 10.3390/f11050564.

J. Rafeeq et al., “Regulation of Phytochemical Properties of Hawthorn: A Crataegus Species,” in Genetic Manipulation of Secondary Metabolites in Medicinal Plant, N. Singh Ravi and Kumar, Ed., Singapore: Springer Nature Singapore, 2023, pp. 179–203. doi: 10.1007/978-981-99-4939-7_8.

A. Cloud, D. Vilcins, and B. McEwen, “The effect of hawthorn (Crataegus spp.) on blood pressure: A systematic re-view,” Adv Integr Med, vol. 7, no. 3, pp. 167–175, 2020, doi: https://doi.org/10.1016/j.aimed.2019.09.002.

E. Kim, E. Jang, and J.-H. Lee, “Potential Roles and Key Mechanisms of Hawthorn Extract against Various Liver Diseases,” Nutrients, vol. 14, no. 4, 2022, doi: 10.3390/nu14040867.

M. Cui et al., “Traditional uses, phytochemistry, pharmacology, and safety concerns of hawthorn (Crataegus genus): A comprehensive review,” J Ethnopharmacol, vol. 319, p. 117229, 2024, doi: https://doi.org/10.1016/j.jep.2023.117229.

W. Guo, T. Shao, Y. Peng, H. Wang, Z.-S. Chen, and H. Su, “Chemical composition, biological activities, and quality standards of hawthorn leaves used in traditional Chinese medicine: a comprehensive review,” Front Pharmacol, vol. 14, 2023, doi: 10.3389/fphar.2023.1275244.

J.-X. Ma et al., “The hawthorn (Crataegus pinnatifida Bge.) fruit as a new dietary source of bioactive ingredients with multiple beneficial functions,” Food Front, vol. 5, no. 4, pp. 1534–1558, 2024, doi: https://doi.org/10.1002/fft2.413.

T. S. Leyane, S. W. Jere, and N. N. Houreld, “Oxidative Stress in Ageing and Chronic Degenerative Pathologies: Molecular Mechanisms Involved in Counteracting Oxidative Stress and Chronic Inflammation,” Int J Mol Sci, vol. 23, no. 13, 2022, doi: 10.3390/ijms23137273.

T. Hertiš Petek and N. Marčun Varda, “Childhood Cardiovascular Health, Obesity, and Some Related Disorders: Insights into Chronic Inflammation and Oxidative Stress,” Int J Mol Sci, vol. 25, no. 17, 2024, doi: 10.3390/ijms25179706.

V. Singh and S. Ubaid, “Role of Silent Information Regulator 1 (SIRT1) in Regulating Oxidative Stress and Inflam-mation,” Inflammation, vol. 43, no. 5, pp. 1589–1598, 2020, doi: 10.1007/s10753-020-01242-9.

P. Yu et al., “N-acetylcysteine Ameliorates Vancomycin-induced Nephrotoxicity by Inhibiting Oxidative Stress and Apoptosis in the in vivo and in vitro Models,” Int J Med Sci, vol. 19, no. 4, p. 740, 2022.

R. Ranasinghe, M. Mathai, and A. Zulli, “Cytoprotective remedies for ameliorating nephrotoxicity induced by renal oxidative stress,” Life Sci, vol. 318, p. 121466, 2023, doi: https://doi.org/10.1016/j.lfs.2023.121466.

L. M. Reguengo, M. K. Salgaço, K. Sivieri, and M. R. Maróstica Júnior, “Agro-industrial by-products: Valuable sources of bioactive compounds,” Food Research International, vol. 152, p. 110871, 2022, doi: https://doi.org/10.1016/j.foodres.2021.110871.

Md. A. Ali et al., “Functional dairy products as a source of bioactive peptides and probiotics: current trends and future prospectives,” J Food Sci Technol, vol. 59, no. 4, pp. 1263–1279, 2022, doi: 10.1007/s13197-021-05091-8.

B. N. Abdul Hakim, N. J. Xuan, and S. N. H. Oslan, “A Comprehensive Review of Bioactive Compounds from Lac-tic Acid Bacteria: Potential Functions as Functional Food in Dietetics and the Food Industry,” Foods, vol. 12, no. 15, 2023, doi: 10.3390/foods12152850.

A. Zeb, “Concept, mechanism, and applications of phenolic antioxidants in foods,” J Food Biochem, vol. 44, no. 9, p. e13394, 2020, doi: https://doi.org/10.1111/jfbc.13394.

B. M. J. and P. T. Enayati Ayesheh and Hatemi, “Plants and Phytochemicals for the Treatment of Atherosclerosis,” in Cardioprotective Plants, S. Pullaiah T. and Ojha, Ed., Singapore: Springer Nature Singapore, 2024, pp. 53–85. doi: 10.1007/978-981-97-4627-9_3.

T. Macedo et al., “Cassia sieberiana DC. leaves modulate LPS-induced inflammatory response in THP-1 cells and inhibit eicosanoid-metabolizing enzymes,” J Ethnopharmacol, vol. 269, p. 113746, 2021, doi: https://doi.org/10.1016/j.jep.2020.113746.

Md. M. Rahaman et al., “Natural antioxidants from some fruits, seeds, foods, natural products, and associated health benefits: An update,” Food Sci Nutr, vol. 11, no. 4, pp. 1657–1670, 2023, doi: https://doi.org/10.1002/fsn3.3217.

H. El-Ramady et al., “Plant Nutrition for Human Health: A Pictorial Review on Plant Bioactive Compounds for Sustainable Agriculture,” Sustainability, vol. 14, no. 14, 2022, doi: 10.3390/su14148329.

N. A. Tahir, J. O. Ahmed, H. A. Azeez, W. R. M. Palani, and D. A. Omer, “Phytochemical, antibacterial, antioxi-dant and phytotoxicity screening of the extracts collected from the fruit and root of wild Mt. Atlas mastic tree (Pis-tacia atlantica subsp. kurdica).,” Appl Ecol Environ Res, vol. 17, no. 2, 2019.

D. Lateef, K. Mustafa, and N. Tahir, “Screening of Iraqi barley accessions under PEG-induced drought conditions,” All Life, vol. 14, no. 1, pp. 308–332, Jan. 2021, doi: 10.1080/26895293.2021.1917456.

N. A. Tahir, K. S. Rasul, D. D. Lateef, and F. M. W. Grundler, “Effects of Oak Leaf Extract, Biofertilizer, and Soil Containing Oak Leaf Powder on Tomato Growth and Biochemical Characteristics under Water Stress Conditions,” Agriculture, vol. 12, no. 12, p. 2082, Dec. 2022, doi: 10.3390/agriculture12122082.

N. A. Tahir and H. A. Azeez, “Antibacterial activity and allelopathic effects of extracts from leaf, stem and bark of Mt. Atlas mastic tree (Pistacia atlantica subsp. kurdica) on crops and weeds,” Allelopathy Journal, vol. 46, no. 1, pp. 121–132, 2019.

F. J. Álvarez-Martínez, E. Barrajón-Catalán, M. Herranz-López, and V. Micol, “Antibacterial plant compounds, extracts and essential oils: An updated review on their effects and putative mechanisms of action,” Phytomedicine, vol. 90, p. 153626, 2021, doi: https://doi.org/10.1016/j.phymed.2021.153626.

F. Nourbakhsh, M. Lotfalizadeh, M. Badpeyma, A. Shakeri, and V. Soheili, “From plants to antimicrobials: Natural products against bacterial membranes,” Phytotherapy Research, vol. 36, no. 1, pp. 33–52, 2022, doi: https://doi.org/10.1002/ptr.7275.

M. C. Lima, C. Paiva de Sousa, C. Fernandez-Prada, J. Harel, J. D. Dubreuil, and E. L. de Souza, “A review of the current evidence of fruit phenolic compounds as potential antimicrobials against pathogenic bacteria,” Microb Pathog, vol. 130, pp. 259–270, 2019, doi: https://doi.org/10.1016/j.micpath.2019.03.025.

R. Biswas, B. Jangra, G. Ashok, V. Ravichandiran, and U. Mohan, “Current Strategies for Combating Biofilm-Forming Pathogens in Clinical Healthcare-Associated Infections,” Indian J Microbiol, vol. 64, no. 3, pp. 781–796, 2024, doi: 10.1007/s12088-024-01221-w.

G. Ozkan, T. Kostka, T. Esatbeyoglu, and E. Capanoglu, “Effects of Lipid-Based Encapsulation on the Bioaccessi-bility and Bioavailability of Phenolic Compounds,” Molecules, vol. 25, no. 23, 2020, doi: 10.3390/molecules25235545.

B. Ramachandran, V. Srinivasadesikan, T.-M. Chou, J. Jeyakanthan, and S.-L. Lee, “Atomistic simulation on flavo-noids derivatives as potential inhibitors of bacterial gyrase of Staphylococcus aureus,” J Biomol Struct Dyn, vol. 40, no. 10, pp. 4314–4327, Jun. 2022, doi: 10.1080/07391102.2020.1856184.

A. Lobiuc et al., “Future Antimicrobials: Natural and Functionalized Phenolics,” Molecules, vol. 28, no. 3, 2023, doi: 10.3390/molecules28031114.

[T. Maliar et al., “Simultaneously Determined Antioxidant and Pro-Oxidant Activity of Randomly Selected Plant Secondary Metabolites and Plant Extracts,” Molecules, vol. 28, no. 19, 2023, doi: 10.3390/molecules28196890.

S. Alfei, G. C. Schito, A. M. Schito, and G. Zuccari, “Reactive Oxygen Species (ROS)-Mediated Antibacterial Oxida-tive Therapies: Available Methods to Generate ROS and a Novel Option Proposal,” Int J Mol Sci, vol. 25, no. 13, 2024, doi: 10.3390/ijms25137182.

J. O. Aribisala, C. E. Aruwa, and S. Sabiu, “Chapter 5 - Progressive approach of phenolic acids toward the ad-vancement of antimicrobial drugs,” in Advancement of Phenolic Acids in Drug Discovery, N. Kumar, N. Goel, and J. S. Gandara, Eds., Academic Press, 2024, pp. 177–210. doi: https://doi.org/10.1016/B978-0-443-18538-0.00004-4.

A. K. Farha et al., “Tannins as an alternative to antibiotics,” Food Biosci, vol. 38, p. 100751, 2020, doi: https://doi.org/10.1016/j.fbio.2020.100751.

S. Manner and A. Fallarero, “Screening of Natural Product Derivatives Identifies Two Structurally Related Flavo-noids as Potent Quorum Sensing Inhibitors against Gram-Negative Bacteria,” Int J Mol Sci, vol. 19, no. 5, 2018, doi: 10.3390/ijms19051346.

R. Pachaiappan et al., “N-acyl-homoserine lactone mediated virulence factor(s) of Pseudomonas aeruginosa inhibit-ed by flavonoids and isoflavonoids,” Process Biochemistry, vol. 116, pp. 84–93, 2022, doi: https://doi.org/10.1016/j.procbio.2022.02.024.

L. Kumar et al., “Molecular Mechanisms and Applications of N-Acyl Homoserine Lactone-Mediated Quorum Sens-ing in Bacteria,” Molecules, vol. 27, no. 21, 2022, doi: 10.3390/molecules27217584.