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Review
.2022 Aug 11:13:973197.
doi: 10.3389/fpls.2022.973197. eCollection 2022.

The genusChrysanthemum: Phylogeny, biodiversity, phytometabolites, and chemodiversity

Affiliations
Review

The genusChrysanthemum: Phylogeny, biodiversity, phytometabolites, and chemodiversity

Da-Cheng Hao et al. Front Plant Sci..

Abstract

The ecologically and economically important genusChrysanthemum contains around 40 species and many hybrids and cultivars. The dried capitulum ofChrysanthemum morifolium (CM) Ramat. Tzvel, i.e.,Flos Chrysanthemi, is frequently used in traditional Chinese medicine (TCM) and folk medicine for at least 2,200 years. It has also been a popular tea beverage for about 2,000 years since Han Dynasty in China. However, the origin of different cultivars of CM and the phylogenetic relationship betweenChrysanthemum and related Asteraceae genera are still elusive, and there is a lack of comprehensive review about the association between biodiversity and chemodiversity ofChrysanthemum. This article aims to provide a synthetic summary of the phylogeny, biodiversity, phytometabolites and chemodiversity ofChrysanthemum and related taxonomic groups, focusing on CM and its wild relatives. Based on extensive literature review and in light of the medicinal value of chrysanthemum, we give some suggestions for its relationship with some genera/species and future applications. Mining chemodiversity from biodiversity ofChrysanthemum containing subtribe Artemisiinae, as well as mining therapeutic efficacy and other utilities from chemodiversity/biodiversity, is closely related with sustainable conservation and utilization of Artemisiinae resources. There were eight main cultivars ofFlos Chrysanthemi, i.e., Hangju, Boju, Gongju, Chuju, Huaiju, Jiju, Chuanju and Qiju, which differ in geographical origins and processing methods. Different CM cultivars originated from various hybridizations between multiple wild species. They mainly contained volatile oils, triterpenes, flavonoids, phenolic acids, polysaccharides, amino acids and other phytometabolites, which have the activities of antimicrobial, anti-viral, antioxidant, anti-aging, anticancer, anti-inflammatory, and closely related taxonomic groups could also be useful as food, medicine and tea. Despite some progresses, the genetic/chemical relationships among varieties, species and relevant genera have yet to be clarified; therefore, the roles of pharmacophylogeny and omics technology are highlighted.

Keywords: Chrysanthemum; Chrysanthemum morifolium; chemodiversity; pharmacophylogeny; phylogenetic relationship; phytochemistry.

Copyright © 2022 Hao, Song, Xiao, Zhong, Wu and Xu.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Phylogenetic relationship of Artemisiinae species, includingChrysanthemum and its wild relatives. The distribution of therapeutic efficacy of ethnomedicinal species on the phylogenetic tree of Chinese taxa is shown. In the inner circle,Artemisia species are in green area, and non-Artemisia species are in red area. From the inside to the outside of the outer circle are poisoning, circulatory diseases, gastrointestinal diseases, nervous system diseases, eye diseases, other/general diseases, hepatobiliary diseases, musculoskeletal diseases, oral diseases, ear/nose/throat diseases, pediatric diseases, reproductive system diseases, respiratory diseases, skin diseases, and urinary diseases, indicated by stars of different colors, square or circle.
Figure 2
Figure 2
Phylogenetic relationship ofChrysanthemum taxa. The number after the taxon name represents the ploidy level. This schematic is compiled mainly based on Shen et al., 2021, as the phylogenetic topology inferred from low-copy nuclear genes and nrITS could be more convincing than those inferred from cp sequences (Liu et al., 2012; Lu et al., 2022a). It should be noted that it is challenging to distinguish taxa from each other withinC. indicum complex andC. zawadskii complex, respectively.
Figure 3
Figure 3
Geographical distribution of representative taxa of Asteraceae subtribe Artemisiinae.(A) GenusAjania is produced in the vast areas of China except the southeast, Mongolia, North Korea, northern Afghanistan and Russia;Opisthopappus is endemic to Taihang Mountains, China;Elachanthemum is distributed in northern China, northwestern China and Mongolia;Hippolytia is produced in central Asia and the Himalayas.(B)C. indicum is produced in Northeast China, North China, Central China, South China, Southwest China, India, Japan, North Korea and Russia;C. vestitum is produced in western Henan, western Hubei and western Anhui, China;C. zawadskii is produced in Heilongjiang, Jilin, Liaoning, Hebei, Shanxi, Inner Mongolia, Shaanxi, Gansu and Anhui of China, Mongolia, Russia and Europe;C. lavandulifolium is produced in Jilin, Liaoning, Hebei, Shandong, Shanxi, Shaanxi, Gansu, Qinghai, Xinjiang (eastern), Jiangxi, Jiangsu, Zhejiang, Sichuan, Hubei and Yunnan of China, Korea and Japan. The geographic distribution data are retrieved from Global Biodiversity Information Facility (https://www.gbif.org/).
Figure 4
Figure 4
Geographical distribution, chemical and morphological characteristics of representative CM cultivars. The medicinal quality (Q) markers of each cultivar are shown: Boju, Huaiju, Gongju and Hangju: chlorogenic acid, 3,5-DCQA, and kaempferol-3-O-rutinoside (Lu et al., 2022b); Chuju: chlorogenic acid, Lut-7-O-G, quercetin, 3,5-DCQA (Yang et al., 2018b); Qiju: chlorogenic acid, 3,5-DCQA, and Lut-7-O-G (Peng et al., 2019); Jiju: chlorogenic acid, luteolin and 3,5-DCQA (Kang et al., 2022). The Q-marker of Chuanju of Zhongjiang, Sichuan Province is not reported. Morphology of medicinal CM: Boju: Inverted conical or cylindrical shape, sometimes slightly flattened and fan-shaped, 1.5–3 cm in diameter, discrete (Chinese Pharmacopoeia Commission, 2020). Involucral bracts dish-shaped; involucral bracts 3–4 layers, ovate or elliptic, herbaceous, yellow-green or brown-green, pubescent outside, margin membranous. Chuju: Irregular spherical or oblate spherical, diameter 1.5–2.5 cm. Ligulate flowers are white, irregularly twisted, involute, with shriveled edges, sometimes with light brown glandular dots; tubular flowers are mostly hidden. Gongju: Oblate spherical or irregular spherical, 1.5–2.5 cm in diameter. Ligulate flowers white or off-white, obliquely ascending, upper part reflexed, margin slightly involute and shriveled, usually without glandular dots; tubular flowers few, exposed. Hangju: It is dish-shaped or oblate spherical, with a diameter of 2.5–4 cm, and is often connected in several pieces. Ligulate flowers white or yellow, spreading or slightly folded, adhering to each other, usually without glandular dots; tubular flowers numerous, exposed. Huaiju: Irregular spherical or oblate spherical, diameter 1.5–2.5 cm. Ligulate flowers are the most, white or yellow, irregularly twisted, involute, with shriveled edges, and sometimes glandular dots can be seen; most of the tubular flowers are hidden.
Figure 5
Figure 5
The molecular structure of representative terpenoid components ofChrysanthemum. A, Monoterpene: camphor, endo-borneol, bornyl acetate, sabinene,1,8-cineole, filifolone, β-myrcene. B, Sesquiterpene: germacrane-type: zawadskinolide F (anti-inflammatory,C. zawadskii), chrysanthediol A (anti-viral, CM); eudesmane-type: chrysanthemumin A (anti-viral,C. indicum), chrysanthemumin D (anti-viral,C. indicum); guaianolide-type: chrysanthemulide A (anti-tumor, anti-inflammatory,C. indicum), cumambrin A (treating osteoporosis,C. ornatum, C. indicum, C. zawadskii); bisabolene-type: jinsidajuol A (CM), tunefulin (C. indicum); others: handelin (anti-aging,C. ornatum, C. indicum), 8,8′-ditigloylchrysanolide D (anti-tumor,C. indicum). C, Triterpene: tetracyclic: stigmastanes: (24R)-saringosterol, (24S)-saringosterol (CM); lanostane: (24S)-lanost-9(11)-ene-3β,24,25-triol (CM); dammaranes: dammarenediol II (CM), 3-epicabraleadiol (anti-viral, CM); cycloartanes: cycloartenol (various bioactivities, CM), (24S)-25-methoxycycloartane-3β,24-diol (anti-inflammatory, CM); tirucallanes: 4,5α-epoxyhelianol (antitubercular, CM), helianol (anti-inflammatory, CM). pentacyclic: lupanes: lupeol (anti-inflammatory,C. indicum, CM), 3-epilupeol (antitubercular, CM); taraxeranes: heliantriol C (anti-tumor, CM), arnidiol (anti-tumor, CM); oleananes: maniladiol (antitubercular, CM), coflodiol (anti-tumor, CM); ursanes:α-amyrin, brein (CM).
Figure 6
Figure 6
The molecular structure of representative flavonoid components of Chrysanthemum. Flavones: Lut-7-O-G (anti-inflammatory, antioxidant, relieving asthma, xanthine oxidase inhibitor, CM,C. indicum), linarin (antioxidant, anti-inflammatory, preventing acute lung injury, promoting osteogenic differentiation, inhibiting acetylcholinesterase activity, CM,C. indicum, C. zawadskii), Api-7-O-(6″-O-acetyl)-β-D-glucopyranoside (antioxidant, CM). Flavonols: kaempferol (antioxidant, anti-inflammatory, anticancer, CM,C. indicum), isorhamnetin 3-O-β-D-G (anti-inflammatory, CM,C. indicum), quercetin 7-O-β-D-G (various bioactivities, CM,C. indicum). C, flavonones: naringenin (treating depression, CM), eriodictyol-7-O-β-D-glucuronide (immunoregulation, C. zawadskii,C. indicum), 5,7,3″,5″-tetrahydroxyflavanone-7-O-β-D-glucopyranoside (C. indicum). D, anthocyanins: cyanidin-3-O-(6″-O-malonyl)glucoside (C. grandiflorum), cyanidin-3-O-(3″,6″-di-O-dimalonyl-β-glucopyranoside)(C. grandiflorum).
Figure 7
Figure 7
The molecular structure of representative phenolic components ofChrysanthemum. chlorogenic acid (=3-CQA), 5-CQA, 3,5-DCQA, 4,5-DCQA, isochlorogenic acid B, 3-O-p-coumaroyl quinic acid, cryptochlorogenic acid, chrysanthemorimic acid A/B/C.
Figure 8
Figure 8
Examples of other phytometabolites ofChrysanthemum. Coumarin, umbelliferone, azelaic acid (C. indicumZou et al., 2022), 4-guanidinobutyric acid, chrysanthelignanoside A (neuroprotection, CM), dendranlignan A (anti-inflammatory, CM), tonghaosu, pyrethrin II, jasmolin II, cinerin I, kamiohnoyneosides A and B (anti-diabetic, CM).
Figure 9
Figure 9
Illustration of pharmacological mechanisms exerted byChrysanthemum extracts and compounds. Various bioactive compounds produced inChrysanthemum plants are shown in left panel; their diverse pharmacological activities and possible mechanisms of action are exemplified in the central part; two representative signaling pathways regulated byChrysanthemum components are shown on the right part. ARE: Antioxidant response element; NF-κB: Nuclear factor kappa-B; Nrf2: NF-E2-related factor 2; TLR4: Toll-like receptor 4.
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