Diversity of antioxidant ingredients among Echinacea species
Graphical abstract
Introduction
The genus Echinacea, belonging to the Asteraceae family, is a group of nine species native to mid-latitude North America (Tang et al., 2017). The distribution of Echinacea covers a wide range of moisture and temperature regimes in North America, from the relative warmth of central Texas, Georgia, and Alabama to the cooler weather of Montana, North Dakota, Minnesota, and Canada (Kindscher, 2016). In the past, Echinacea was used by Native Americans for various ailments, including mouth sores, colds, and cough (Borchers et al., 2000). Echinacea-derived products are widely used as daily supplements worldwide and are marketed and used as immunostimulants to treat and prevent the common cold, influenza, and upper respiratory tract infections (Cao and Kindscher, 2016). Owing to the health benefits, products from Echinacea have drawn increasing attention globally and have become a massive industry. In 2019, in the US market alone, the sales of products from three commonly used species, including E. angustifolia (Ean), E. pallida (Epa), and E. purpurea (Epu) reached 120 million US dollars, an increase of 4.9% compared with the previous year. In addition, in the first half of 2020, Echinacea sales grew sharply by 90.9%, which may be due to the COVID-19 pandemic (Smith et al., 2020).
Modern pharmacology studies on Echinacea have identified many bioactivities, such as antioxidant, immunomodulatory, anti-inflammatory, antifungal, and antiviral activities (Barrett, 2003; Binns et al., 2002; Melchart et al., 1995). Caffeic acid derivatives, alkamides, polysaccharides, polyacetylenes, polyenes, flavonoids, and terpenoids have been linked to these bioactivities (Cao and Kindscher, 2016). In addition, synergistic effects of alkamides, caffeic acid derivatives, and polysaccharides have been reported in E. purpurea (Dalby-Brown et al., 2005). Two important caffeic acid derivatives from Echinacea, chicoric acid and echinacoside, have been widely studied for the remarkable bioactivity and are assumed to be the active ingredients of Echinacea (Aiello et al., 2015; Naveed et al., 2018; Silva et al., 2014). The production, stabilization, and changes during storage have been extensively studied (Bergeron et al., 2002; Dalby-Brown et al., 2005; Lin et al., 2011). The chemical compositions of the three commonly used Echinacea species (Ean, Epa, and Epu) were different, resulting in various bioactivities (Barnes et al., 2010; Erenler et al., 2015; Perry et al., 2001; Sloley et al., 2001; Thomsen et al., 2012). On a broader level, the genome size and chloroplast genome of the Echinacea genus have been compared (Jedrzejczyk, 2020; Zhang et al., 2017).
Recently, the complete biosynthesis pathway of chicoric acid in Echinacea has been successfully elucidated (Fu et al., 2021). Chicoric acid and its two substrates, caftaric acid and chlorogenic acid, originate from phenylpropanoid metabolism. Hydroxycinnamoyl-CoA: quinate/shikimate hydroxycinnamoyl transferase (HCT) catalyzes the synthesis of caffeoyl CoA, the most important precursor; hydroxycinnamoyl-CoA: tartaric acid hydroxycinnamoyl transferase (HTT) catalyzes caffeoyl CoA and tartaric acid to synthesize caftaric acid; hydroxycinnamoyl-CoA: quinate hydroxycinnamoyl transferase (HQT) combines caffeoyl CoA and quinic acid into chlorogenic acid; and caftaric acid and chlorogenic acid are used as acyl acceptor and acyl donor, respectively, by chicoric acid synthase (CAS) to generate chicoric acid. These four biosynthetic enzymes complete the specific chicoric acid biosynthesis and allow the study of the intrinsic determinants of chicoric acid diversity in Echinacea (Fu et al., 2021).
In the present study, the chemical differences among six Echinacea species, namely, Epu, Epa, Ean, E. atrorubens (Eat), E. paradoxa var. paradoxa (Epp), and E. sanguinea (Esa), were compared using non-target metabolomics. The active antioxidant ingredients were determined based on the positive relationship between the observed antioxidant activity and the sum of each active ingredient’s antioxidant contribution. Finally, the potential mechanisms of chicoric acid and caftaric acid diversity among Echinacea species were investigated. All these results will significantly promote the research into Echinacea species, such as the selection of materials for special applications.
Section snippets
Reagents
MS-grade methanol, acetonitrile, and formic acid were purchased from Thermo Fisher Scientific Inc. (MA). Chlorogenic acid (98%, CAS: 327-97-9) was obtained from Chengdu Herbpurify Co., Ltd. (Chengdu, China). Caftaric acid (98%, CAS: 67879-58-7), chicoric acid (98%, CAS: 6537-80-0), echinacoside (98%, CAS: 82854-37-3), fluorescein sodium salt, 2,2′-azobis (2-methylpropionamidine) dihydrochloride (AAPH), 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), potassium
The chemical diversity of Echinacea species
Six of the nine known Echinacea species, namely, Epu, Epa, Ean, Eat, Epp, and Esa were germinated and cultivated in a greenhouse under the same conditions for 2 months. The phenotypes of the Echinacea species are shown in Fig. 1a. Among them, Epu showed a distinct phenotype with more fibrous roots and wide blades. The aerial parts and roots were separately extracted and analyzed.
First, a liquid chromatography-high resolution mass spectrometry (LC-HRMS)-based non-target metabolomic analysis was
Conclusion
Echinacea species have received increasing attention owing to the health benefits and great potential for industrial applications. Diversity in chemical composition exists within the genus. In the present study, Echinacea species were cultivated under the same conditions to exclude environmental effects on the chemical contents. The chemical diversity was comprehensively studied and analyzed. Echinacea sanguinea has considerable potential for the production of chicoric acid, in addition to the
CRediT authorship contribution statement
Rao Fu: Conceptualization, Methodology, Investigation, Resources, Data curation, Writing - original draft, Writing - review & editing, Visualization, Project administration, Funding acquisition. Pingyu Zhang: Methodology, Investigation, Resources. Zongbi Deng: Methodology, Investigation, Resources. Ge Jin: Methodology, Investigation, Resources. Yiran Guo: Conceptualization, Writing - review & editing, Project administration, Funding acquisition. Yang Zhang: Conceptualization, Writing - review &
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
This work was financially supported by the Natural Science Foundations of China (No. 31800258 and 31670352) and the China Postdoctoral Science Foundation Grant (No. 2018M631080).
References (40)
- et al.
Harvest in different years of growth influences chemical composition of Echinacea angustifolia roots
Ind. Crop. Prod.
(2015) Medicinal properties of Echinacea: a critical review
Phytomedicine
(2003)- et al.
Effect of antioxidant oxidation potential in the oxygen radical absorption capacity (ORAC) assay
Food Chem.
(2008) - et al.
Inflammation and Native American medicine: the role of botanicals
Am. J. Clin. Nutr.
(2000) Acyltransferases in plants: a good time to be BAHD
Curr. Opin. Plant Biol.
(2006)- et al.
Antioxidant and anti-inflammatory activities of the phenolic extracts of Sapium sebiferum (L.) Roxb. leaves
J. Ethnopharmacol.
(2013) - et al.
Determination of phenolic contents and antioxidant activities of extracts of Jatropha curcas L. seed shell, a by-product, a new source of natural antioxidant
Ind. Crop. Prod.
(2014) - et al.
Chemical composition, antioxidant and antimicrobial activity of Chinese tallow tree leaves
Ind. Crop. Prod.
(2015) - et al.
Hepatoprotection using Brassica rapa var. rapa L. seeds and its bioactive compound, sinapine thiocyanate, for CCl4-induced liver injury
J. Funct. Foods
(2016) Genome size and SCoT markers as tools for identification and genetic diversity assessment in Echinacea genus
Ind. Crop. Prod.
(2020)
Effect of drying and storage conditions on caffeic acid derivatives and total phenolics of Echinacea purpurea grown in Taiwan
Food Chem.
Chlorogenic acid (CGA): a pharmacological review and call for further research
Biomed. Pharmacother.
Analysis of phenolic compounds and radical scavenging activity of Echinacea spp
J. Pharm. Biomed. Anal.
Ultrasound-assisted deep eutectic solvent extraction of echinacoside and oleuropein from Syringa pubescens Turcz
Ind. Crop. Prod.
Separation and purification of echinacoside from Penstemon barbatus (Can.) Roth by recycling high-speed counter-current chromatography
J. Chromatogr. B.
Echinacea species (Echinacea angustifolia (DC.) Hell., Echinacea pallida (Nutt.) Nutt., Echinacea purpurea (L.) Moench): a review of their chemistry, pharmacology and clinical properties
J. Pharm. Pharmacol.
Stabilization of caffeic acid derivatives in Echinacea purpurea L. glycerin extract
J. Agric. Food Chem.
Antiviral activity of characterized extracts from Echinacea spp. (Heliantheae: Asteraceae) against Herpes simplex Virus (HSV-I)
Planta Med.
BAHD or SCPL acyltransferase? What a dilemma for acylation in the world of plant phenolic compounds
New Phytol.
The medicinal chemistry of Echinacea species
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