Influence of climate variation on phenolic composition and antioxidant capacity of Medicago minima populations

[en] Medicago minima is a pasture legume that grows almost all over the world. In Tunisia, it occupies various climatic environments and is considered the most abundant annual Medicago plant. However, this species is unconsumed and unused by humans. This study aimed to explore the phytochemical characteristics of Medicago minima selected from diferent provenances in Tunisia and subsequently investigate the infuence of environmental factors on their phenolic composition and antioxidant activity. Therefore, a calorimetric method and DPPH tests provided the total phenolic and totalfavonoid contents and antioxidant potential in roots, stems, leaves and seeds. High performance liquid chromatography (HPLC) identifed and quantifed four phenolic acids and three favonoids in the studied organs. Roots and leaves showed the greatest phenolic compound content and had high antioxidant activity. Rutin and syringic acid (leaves) represent a characteristic for this species. For each organ, principal component analysis of phenolic profles showed that the root’s phenolic composition could be an indication of the plant adaptation to even small changes in its environments. Plants originating from a cold climate, higher altitude or semi-arid environment had the highest phenolic compound contents in their organs. Our fndings provide useful information for the exploitation of the phenolic compounds in these weeds for the development of environmental sustainability.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)
Chemistry

Author, co-author :

Kabtni, Souhir

Sdouga, Dorra

Bettaieb Rebey, Iness

Saive, Matthew ; Université de Liège - ULiège > Terra

Trifi-Farah, Neila

Fauconnier, Marie-Laure ; Université de Liège - ULiège > Département GxABT > Chimie des agro-biosystèmes

Marghali, Sonia

Language :

English

Title :

Influence of climate variation on phenolic composition and antioxidant capacity of Medicago minima populations

Publication date :

May 2020

Journal title :

Scientific Reports

eISSN :

2045-2322

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

Pages :

8293

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.nature.com/articles/s41598-020-65160-4

Funders :

Tunisian Ministry of Higher Education (research grants Scholarship of September 2017)

Available on ORBi :

since 20 May 2020

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Bibliography

Rodrigues, F., Almeida, I., Sarmento, B., Amaral, M. H. & Oliveira, M. B. Study of the isoflavone content of different extracts of Medicago spp. as potential active ingredient. Industrial Crops and Products 57, 110–115, 10.1016/j.indcrop.2014.03.014 (2014).
Barreira, J. C. et al. Medicago spp. as potential sources of bioactive isoflavones: Characterization according to phylogenetic and phenologic factors. Phytochemistry 116, 230–238, 10.1016/j.phytochem.2015.04.011 (2015).
Visnevschi‐Necrasov, T. et al. Advances in isoflavone profile characterisation using matrix solid‐phase dispersion coupled to HPLC/DAD in Medicago species. Phytochemical analysis 26(1), 40–46, 10.1002/pca.2534 (2015).
Connor, A. M., Finn, C. E. & Alspach, P. A. Genotypic and environmental variation in antioxidant activity and total phenolic content among blackberry and hybridberry cultivars. Journal of the American Society for Horticultural Science 130(4), 527–533 (2005).
Crozier, A., Clifford, M. N. & Ashihara, H. Plant secondary metabolites. Occurrence, Structure and Role in the Human Diet. (Blackwell-Publishers, 2006)., 10.1002/9780470988558
Chebouti, A., Bekki, A., Mefti, M. & Meziani, N. Characterization and Agronomic Evaluation of Local Populations of M. minima (L.) Collected in Algerian Steppe Area. Journal of Agronomy 14(4), 212–219 (2015).
Dölarslan, M., Gül, E. & Erşahin, S. Endemic Vascular Plants of Marble and Serpentine Parent Materials in Semiarid Grassland. Turkish Journal of Agriculture - Food Science and Technology 6(6), 693–698, 10.24925/turjaf.v6i6.693-698.1703 (2018).
Small, E. Alfalfa and Relatives: Evolution and Classification of Medicago. (NRC Research Press, 2011). ISBN: 0660199793, 9780660199795
Woods, M., Orcutt, J. The genus Medicago (Fabaceae) in Alabama. Phytoneuron 2017 (52), 1–17 ISSN 2153 733X (2017).
Zoghlami, A., Hassen, H., Seklani, H., Robertson, L. & Salkini, A. K. Distribution des luzernes annuelles en Tunisie centrale en fonction des facteurs édaphiques et climatiques. Fourrages 145, 5–16 (1996).
Ahuja, I., De Vos, R. C., Bones, A. M. & Hall, R. D. Plant molecular stress responses face climate change. Trends in plant science 15(12), 664–674, 10.1016/j.tplants.2010.08.002 (2010).
Holopainen, J. K., et al Climate change effects on secondary compounds of forest trees in the northern hemisphere. Frontiers in plant science 9, 10.3389/fpls.2018.01445 (2018).
Parida, A. K., Dagaonkar, V. S., Phalak, M. S., Umalkar, G. V. & Aurangabadkar, L. P. Alterations in photosynthetic pigments, protein and osmotic components in cotton genotypes subjected to short-term drought stress followed by recovery. Plant Biotechnol. Rep 1, 37–48 (2007).
Rathee, P. et al. Mechanism of action of flavonoids as anti-inflammatory agents: a review. Inflammation & allergy-drug targets (formerly current drug targets-inflammation & allergy) 3, 229–235 (2009).
Tungmunnithum, D., Thongboonyou, A., Pholboon, A. & Yangsabai, A. Flavonoids and other phenolic compounds from medicinal plants for pharmaceutical and medical aspects: An overview. Medicines 5(3), 93, 10.3390/medicines5030093 (2018).
Chaalal, M. et al. Phenolic contents and in vitro antioxidant activity of four commonly consumed nuts in algeria. Acta Alimentaria 48(1), 125–131, 10.1556/066.2018.0009 (2019).
Ortega‐Ramirez, L. A. et al. Potential of medicinal plants as antimicrobial and antioxidant agents in food industry: a hypothesis. Journal of food science 79(2), 129–137 (2014).
He, G. R., Wang, S. B. & Du, G. H. Natural Small Molecule Drugs from Plants. Part VII, 703-707. (Springer, Singapore 2018). 10.1007/978-981-10-8022-7_114
Rao, P. S., Satelli, A., Moridani, M., Jenkins, M. & Rao, U. S. Luteolin induces apoptosis in multidrug resistant cancer cells without affecting the drug transporter function: Involvement of cell line‐specific apoptotic mechanisms. International journal of cancer 130(11), 2703–2714, 10.1002/ijc.26308 (2012).
Chen C. Sinapic acid and its derivatives as medicine in oxidative stress-induced diseases and aging. Oxidative medicine and cellular longevity 2016, 10.1155/2016/3571614 (2016).
Periyannan, V. & Veerasamy, V. Syringic acid may attenuate the oral mucosal carcinogenesis via improving cell surface glycoconjugation and modifying cytokeratin expression. Toxicology reports 5, 1098–1106, 10.1016/j.toxrep.2018.10.015 (2018).
Srinivasulu, C., Ramgopal, M., Ramanjaneyulu, G., Anuradha, C. M. & Kumar, C. S. Syringic acid (SA)‒A Review of Its Occurrence, Biosynthesis, Pharmacological and Industrial Importance. Biomedicine & Pharmacotherapy 108, 547–557, 10.1016/j.biopha.2018.09.069 (2018).
Guerrero, J. L. G., Guirado, C. M., Fuentes, M. M. R. & Pérez, A. C. Nutrient composition and antioxidant activity of 10 pepper (Capsicum annuun) varieties. European Food Research and Technology 224, 1–9, 10.1007/s00217-006-0281-5 (2006).
Rodrigues, F. et al. Medicago spp. extracts as promising ingredients for skin care products. Industrial crops and products 49, 634–644, 10.1016/j.indcrop.2013.06.015 (2013).
Martínez, R. et al. Medicago sativa L., a functional food to relieve hypertension and metabolic disorders in a spontaneously hypertensive rat model. Journal of Functional. Foods 26, 470–484 (2016).
Krakowska, A., Rafińska, K., Walczak, J., Kowalkowski, T. & Buszewski, B. Comparison of various extraction techniques of Medicago sativa: yield, antioxidant activity, and content of phytochemical constituents. Journal of AOAC International 100(6), 1681–1693, 10.5740/jaoacint.17-0234 (2017).
Soumaya, K., Chaouachi, F., Ksouri, R. & El Gazzah, M. Polyphenolic composition in different organs of Tunisia populations of Cynara cardunculus L. and their antioxidant activity. J. Food Nutr. Res. 1, 1–6, 10.12691/jfnr-1-1-1 (2013).
Falleh, H. et al. Phenolic composition of Cynara cardunculus L. organs, and their biological activities. Comptes Rendus Biologies 331(5), 372–379, 10.1016/j.crvi.2008.02.008 (2008).
Maj, D., Wielbo, J., Marek-Kozaczuk, M. & Skorupska, A. Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiological research 165(1), 50–60 (2010).
Mandal, S. M., Chakraborty, D. & Dey, S. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant signaling & behavior 5(4), 359–368 (2010).
Wink, M. Evolution of secondary metabolites in legumes (Fabaceae). South African Journal of Botany 89, 164–175 (2013).
Gargallo-Garriga, A. et al. Root exudate metabolomes change under drought and show limited capacity for recovery. Scientific reports 8(1), 12696 (2018).
Kowalska, I. et al. Flavonoids from barrel medic (Medicago truncatula) aerial parts. Journal of agricultural and food chemistry 55(7), 2645–2652 (2007).
Karimi, E. et al. Insight into the functional and medicinal properties of Medicago sativa (Alfalfa) leaves extract. Journal of Medicinal Plants Research 7(7), 290–297, 10.5897/JMPR11.1663 (2013).
Ganeshpurkar, A. & Saluja, A. K. The pharmacological potential of rutin. Saudi pharmaceutical journal 25(2), 149–164 (2017).
Ha, S. J. et al. Syringic acid prevents skin carcinogenesis via regulation of NoX and EGFR signaling. Biochemical pharmacology 154, 435–445, 10.1016/j.bcp.2018.06.007 (2018).
Srinivasan, M., Sudheer, A. R. & Menon, V. P. Ferulic acid: therapeutic potential through its antioxidant property. Journal of clinical biochemistry and nutrition 40(2), 92–100 (2007).
Kumar, N. & Pruthi, V. Potential applications of ferulic acid from natural sources. Biotechnology Reports 4, 86–93, 10.1016/j.btre.2014.09.002 (2014).
Khang, D., Dung, T., Elzaawely, A. & Xuan, T. Phenolic profiles and antioxidant activity of germinated legumes. Foods 5(2), 27 (2016).
Cheung, Y., Meenu, M., Yu, X. & Xu, B. Phenolic acids and flavonoids profiles of commercial honey from different floral sources and geographic sources. International Journal of Food Properties 22(1), 290–308, 10.1080/10942912.2019.1579835 (2019).
Ferreres, F. et al. HPLC-DAD-ESI/MSn profiling of phenolic compounds from Lathyrus cicera L. seeds. Food chemistry 214, 678–685 (2017).
Kritsadaruangchai, U. et al. Effect of solid state fermentation with Trichoderma spp. on phenolic content and antioxidant capacities of mature Assam tea leaves. Journal of Food Science and Agricultural Technology (JFAT) 5, 106–113, http://rs.mfu.ac.th/ojs/index.php/jfat (2019).
Ercisli, S., Orhan, E., Ozdemir, O. & Sengul, M. The genotypic effects on the chemical composition and antioxidant activity of sea buckthorn (Hippophae rhamnoides L.) berries grown in Turkey. Scientia Horticulturae 115(1), 27–33, 10.1016/j.scienta.2007.07.004 (2007).
Scalzo, J., Politi, A., Pellegrini, N., Mezzetti, B. & Battino, M. Plant genotype affects total antioxidant capacity and phenolic contents in fruit. Nutrition 21(2), 207–213, 10.1016/j.nut.2004.03.025 (2005).
Capocasa, F., Scalzo, J., Mezzetti, B. & Battino, M. Combining quality and antioxidant attributes in the strawberry: The role of genotype. Food Chemistry 111(4), 872–878, 10.1016/j.foodchem.2008.04.068 (2008).
Dong, X., Hu, Y., Li, Y. & Zhou, Z. The maturity degree, phenolic compounds and antioxidant activity of Eureka lemon [Citrus limon (L.) Burm. f.]: A negative correlation between total phenolic content, antioxidant capacity and soluble solid content. Scientia Horticulturae 243, 281–289, 10.1016/j.scienta.2018.08.036 (2019).
Dolkar, P., Dolkar, D., Angmo, S., Kumar, B. & Stobdan, T. Variability in phenolics, flavonoids and antioxidants in seabuckthorn (Hippophae rhamnoides L.) seed from nine trans-Himalayan natural population. Journal of Berry Research 7(2), 109–116, 10.3233/JBR-170149 (2017).
Zhang, J., Chen, G., Zhao, P., Zhou, Q. & Zhao, X. The abundance of certain metabolites responds to drought stress in the highly drought tolerant plant Caragana korshinskii. Acta Physiol. Plant 39 (2017).
Khaosaad, T. et al. Effect of mycorrhization on the isoflavone content and the phytoestrogen activity of red clover. Journal of plant physiology 165(11), 1161–1167 (2008).
Vives-Peris, V., De Ollas, C., Gómez-Cadenas, A. & Pérez-Clemente, R. M. Root exudates: from plant to rhizosphere and beyond. Plant cell reports 1–15 (2019).
Weidner, S. et al. Phenolic compounds and properties of antioxidants in grapevine roots [Vitis vinifera L.] under low-temperature stress followed by recovery. Acta Societatis Botanicorum Poloniae 78(4), 279–286 (2009).
Aninbon, C. et al. Effect of end of season water deficit on phenolic compounds in peanut genotypes with different levels of resistance to drought. Food chemistry 196, 123–129 (2016).
Zhang, Z. Z. et al. Three types of ultraviolet irradiation differentially promote expression of shikimate pathway genes and production of anthocyanins in grape berries. Plant Physiology and Biochemistry 57, 74–83 (2012).
Naikoo, M. I. et al. Plant Signaling Molecules. Chapter 9, 157–168, 10.1016/B978-0-12-816451-8.00009-5 (Woodhead Publishing, 2019).
Pfeifer, M. T., Koepke, P. & Reuder, J. Effects of altitude and aerosol on UV radiation. Journal of Geophysical Research: Atmospheres 111(D1), https://doi.org/10.1029/2005JD006444 (2006).
Liu, W. et al. Influence of environmental factors on the active substance production and antioxidant activity in Potentilla fruticosa L. and its quality assessment. Scientific reports 6, 28591, 10.1038/srep28591 (2016).
Samanta, A., Das, G., & Das, S. K. Roles of flavonoids in plants. Carbon 100(6) (2011).
Sano, N. et al. Staying alive: molecular aspects of seed longevity. Plant and Cell Physiology 57(4), 660–674 (2015).
MacGregor, D. R. et al. Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. New Phytologist 205(2), 642–652 (2015).
Benini, C. et al. Comparative Chemical and Molecular Variability of Cananga odorata (Lam.) Hook.f. Thomson forma genuina (Ylang-Ylang) in the Western Indian Ocean Islands: Implication for Valorization. Chemistry and Biodiversity 9(7), 1389–1402, 10.1002/cbdv.201100306 (2012).
Figueiredo, A. C., Barroso, J. G., Pedro, L. G. & Scheffer, J. J. Factors affecting secondary metabolite production in plants: volatile components and essential oils. Flavour and Fragrance Journal 23(4), 213–226, 10.1002/ffj.1875 (2008).
Zhu, Z. et al. Ultrasound-assisted extraction, centrifugation and ultrafiltration: Multistage process for polyphenol recovery from purple sweet potatoes. Molecules 21(11), 1584, 10.3390/molecules21111584 (2016).
Gîrd, C. E. et al. research regarding obtaining herbal extracts with antitumour activity. Note ii. Phytochemical analysis, antioxidant activity and cytotoxic effects of Chelidonium majus., Medicago sativa. and Berberis vulgaris. Dry Extracts. Chelidonium Majus 2017, 703–708 (2017).
Riffault, L., Destandau, E., Pasquier, L., André, P. & Elfakir, C. Phytochemical analysis of Rosa hybrida cv.‘Jardin de Granville’by HPTLC, HPLC-DAD and HPLC-ESI-HRMS: Polyphenolic fingerprints of six plant organs. Phytochemistry 99, 127–134, 10.1016/j.phytochem.2013.12.015 (2014).
Hoff, J. E. & Singleton, K. I. A method for determination of tannins in foods by means of immobilized protein. Journal of Food Science 42(6), 1566–1569, 10.1111/j.1365-2621.1977.tb08427.x (1977).
Woisky, R. G. & Salatino, A. Analysis of propolis: some parameters and procedures for chemical quality control. Journal of Apiculture Research 37, 99–105, 10.1080/00218839.1998.11100961 (1998).
Sánchez-Moreno, C., Larrauri, J. A., Saura-Calixto, F. A procedure to measure the antiradical efficiency of polyphenols. Journal of the Science of Food and Agriculture 76, 270–276 10.1002/(SICI)1097-0010(199802)76:2<270::AID-JSFA945>3.0.CO;2-9 (1998).
R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Austria 2015, https://www.R-project.org/ (2018).
Fox, J. Getting started with the R commander: a basic-statistics graphical user interface to R. J Stat Softw. 14(9), 1–42 (2005).
Fox, J. Using the R Commander: A Point-and-Click Interface for R. Chapman and Hall/CRC, (New York, 2016).
De Mendiburu, F. agricolae: Statistical Procedures for Agricultural Research. R package version 1.2-8., https://CRAN.R-project.org/package=agricolae (2017).