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2022 Volume 2
Article Contents
Abstract
Introduction
Data source and search strategy
Publication collection and exclusion criteria
Publication contribution analysis
Scientific production
Data analysis and findings
Summary of review
Conclusions
Limitations and future research agenda
Author contributions
Data availability
Conflict of interest
Supplementary information
Rights and permissions
References
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ARTICLE   Open Access    

Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny

  • 1.

    Institute of Grassland, Flowers and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center of Functional Floriculture, Beijing 100097, China

  • 2.

    College of Landscape Architecture, Sichuan Agricultural University, Chengdu 611130, China

  • 3.

    College of Landscape Architecture, Beijing University of Agriculture, Beijing 100097, China

  • 4.

    Chengdu Landscape Architecture Planning & Designing Institute, Chengdu Park City Research Center, Chengdu 610036, China

  • 5.

    Institute of Agri-food Processing and Nutrition (IAPN), Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China

  • # These authors contributed equally: Hua Liu, Xiaoxi Chen

More Information
  • Chrysanthemum and Opisthopappus are genera that include perennial herbaceous floral species, including excellent varieties with strong fragrances resulting from long-term artificial selection. Thus, they are ornamentally and economically important flower resources. In this study, a water distillation method was used to extract essential oils from the inflorescences of Chrysanthemum and Opisthopappus wild resources and hybrid progeny with high essential oil contents (Chrysanthemum morifolium 'xiangjin', C. morifolium 'xiangyun', C. morifolium 'xinjiboju', Opisthopappus taihangensis, Opisthopappus longilobus, Chrysanthemum lavandulifolium, and C. morifolium 'minghuangju'). The essential oil extraction rates were as follows: 1.17‰, 2‰, 1.67‰, 2.17‰, 0.43‰, 1‰, and 1.17‰. On the basis of HS-SPME-GC-MS (Headspace solid phase microextraction-gas chromatography-mass spectrometry), 225 volatile compounds were detected in the seven analyzed essential oil samples. Each essential oil had a relative volatile component content exceeding 0.3. The three most abundant compounds were olefins (46 types), alcohols (34 types), and esters (18 types). The volatile components with relatively high contents included thymol, D-camphor, pinene, eucalyptol, 2-terpineol, terpineol, trans-caryophyllene, and β-elemene. These volatile compounds have strong biological activities and are useful components of medicines and daily-use products. An evaluation of their antibacterial effects demonstrated that the essential oils of C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, and C. 'minghuangju' inhibited the growth of Escherichia coli. The C. lavandulifolium essential oil inhibited the growth of Pectobacterium carotovorum. The results of this study will provide researchers with an important theoretical basis for the development and application of Chrysanthemum and Opisthopappus essential oils.

  • Introduction

    The Trichoderma genus encompasses a wide-ranging collection of filamentous fungi, prevalent in various natural ecosystems[1]. Trichoderma species within this genus have earned acclaim for their exceptional capacity to inhabit plant roots, stimulate plant growth, and showcasing biocontrol attributes against a spectrum of fungal adversaries[2]. Employing tactics like mycoparasitism, antibiosis, competitive resource acquisition, and plant resistance induction, these species effectively manage fungal diseases[3]. Notably, they are increasingly utilized in agriculture as biofertilizers and biopesticides[1]. Trichoderma-based bio-fungicides, available in different formulations like wettable powders, granules, and flowable concentrates, offer a convenient application to seeds, seedlings, soil, and foliage[4,5]. Besides their disease-fighting properties, these bio-fungicides promote plant growth through various mechanisms such as phytohormone production, nutrient solubilization, and stress tolerance enhancement[3]. Recent progress in Trichoderma-based formulations has led to innovative materials, advanced nanotechnology strategies, and genetic engineering techniques aimed at boosting stability, shelf life, and efficacy[4]. Among these advancements, biochar has shown promise as an ideal carrier for Trichoderma formulations due to its high porosity, surface area, and soil stability maintenance abilities[6]. New research indicates that biochar can strengthen Trichoderma's biocontrol properties[7,8]. Experiments show that using Trichoderma bio-fungicides on soil blended with biochar is more effective in fungal disease control than on unamended earth[9]. Likewise, applying these bio-fungicides on biochar-coated seeds provides better resistance against fungal diseases in seedlings[7,10]. Such biotechnological advancements in Trichoderma-based formulations can promote sustainable agricultural practices by reducing reliance on chemical pesticides[11]. This, in turn, helps mitigate the ecological impact of agricultural activities and enhances food and feed safety[12]. By protecting plants from fungal diseases and improving soil fertility, Trichoderma-based bio-fungicides hold promise for enhancing crop yield[1]. Trichoderma formulations play a crucial role in minimizing harm to non-target organisms while maximizing the effectiveness of the active ingredient[13]. While Trichoderma is significant in ensuring agronomic safety, challenges in their formulation persist due to potential degradation of the biomass or bioactive metabolite caused by factors like exposure to air, light, and temperature[14]. Additionally, these products need to be easy to handle, apply, and produce[15,16]. To address this objective, the present study aims to offer a comprehensive examination of various technological advancements that enhance the efficiency of natural preparations. Distinguishing itself from typical literature reviews that predominantly delve into the biological attributes of metabolites, this review incorporates a bibliometric analysis of biopesticides and their formulations[17]. This analysis employs quantitative and statistical indicators to identify patterns related to the most critical pest issues, agriculture's susceptibility, sources of biological control, innovative methodologies, and the current status of Trichoderma formulations. The insights presented in this analysis significantly contribute to the bibliometric methodology, potentially promoting positive strides in the advancement of technology for Trichoderma formulation. Additionally, it offers valuable suggestions for researchers engaged in this field.

    Bibliometric analysis is a technique employed to scrutinize the characteristics and evolving patterns within academic literature using various mathematical and statistical methods[10]. Through this approach, we can quantitatively assess the overall state of the literature, collaborative relationships, research areas of interest, and the development trends in a specific research field[18]. A descriptive analysis of the corpus of published research pertaining to Trichoderma formulations was conducted. This analysis entailed the examination of co-occurring terms within the body of published articles, allowing for the elucidation of evolutionary trends in scientific themes[19]. The fundamental aim of this research is to conduct an exhaustive review of the existing body of literature on Trichoderma formulations and to project the areas of highest interest and potential for future investigation[20]. One of the primary objectives of bibliometric analysis is to assess the trends in research related to Trichoderma formulations, and to identify the most influential authors and institutions in the field of Trichoderma research. Determining the impact of research in terms of citations, patents, or applications in real-world scenarios.

    As a result, this study seeks to investigate the following research objectives: In the field of Trichoderma formulations, what are the key research themes and trends observed from 2016 to 2023 include:

    (1) How is research on Trichoderma formulations distributed geographically, and what regions exhibit the most active contributions to the field? (2) Can bibliometric analysis predict future trends and potential innovations in Trichoderma formulations research based on historical patterns? (3) The article follows a well organised structure[21]. Initially the research methodology adopted for the study is outlined. Subsequently, a well-organized article is crucial for effectively communicating research findings to the intended audience[22].

    Data source and search strategy

    Literature retrieval was performed online through the Science Citation Index Expanded (SCI-E) of the Web of Science Core Collection (WoSCC, Clarivate Analytics) from 2016 to 2023[21,22]. Scopus is a preferred data source for bibliometric analysis, and it provides comprehensive information and data from a multi-disciplinary field of literature[23]. To retrieve literature comprehensively and accurately on Trichoderma formulations, different search terms and retrieval strategies were assembled in this study. Finally, the optimal search items were set as follows: TS = ('Trichoderma formulation*') OR ('Bio formulation of Trichoderma*') OR ('Bio control') OR ('Antagonist') OR ('Rhizosphere fungus')[24]. The data range was set from 2016 to 2023, to collect all relevant publications. It is worth noting that as the Scopus database data network is constantly updated, the results may vary depending on the exact retrieval date.

    A detailed literature retrieval process was performed online through Science Citation Index Expanded (SCI-E) of the Web of Science Core Collection (WoSCC, Clarivate Analytics) from 2016 to 2023, and considered Scopus as a preferred data source for bibliometric analysis. Additionally, we outlined the search terms and retrieval strategies that are used in our study and set the range of data from 2016 to 2023 to collect all relevant publications. If we sum up our descriptions narrate on the following key points, like data sources, search terms, data range, constantly updated data base, and optimal search items[25]. The search strategy was designed to capture relevant literature on Trichoderma formulations. The search terms included Trichoderma formulation, bio-formulation of Trichoderma, biocontrol, antagonist and Rhizosphere fungus. The asterisks, in the search terms are used as wildcard characters to capture different word endings. The data range was set from 2016 to 2023 to collect all relevant publications within that timeframe. This was the period during which the literature retrieval was performed[25]. It is mentioned that as the Scopus database data network is constantly updated, and the results may vary depending on the exact retrieval date. This indicates that the study acknowledged the dynamic nature of the database and its potential impact on the results[26]. After assembling different search terms and retrieval strategies, the study determined the optimal search items, which were the selected search terms that would yield the most comprehensive and accurate results for the study's objectives. Overall, the present study took a systematic approach to literature retrieval, considering multiple data sources and employing a combination of search terms to ensure the retrieval of relevant publications on Trichoderma formulations. It is worth noting that as the Scopus database data network is constantly updated, to add upon, the results may vary depending on the exact retrieval date.

    Publication collection and exclusion criteria

    To ensure the credibility of the research conclusions, this study gathered peer-reviewed English journal articles to summarize global research perspectives. It's important to mention that articles not aligned with this paper's purpose were manually omitted in the final phase of data collection[27]. For instance, some articles explored the relationship between plants and microorganisms on leaves. Eventually, a total of 287 articles that met all criteria were sourced from Scopus. These pieces represented almost all top-tier experimental studies on Trichoderma formulations from 2016 to 2023 worldwide. The variability among these articles could effectively indicate the trend of related research development. Therefore, these publications were prioritized for further analysis and assessment. Figure 1 illustrates the flowchart of the literature retrieved in this study[28].

    Figure 1.  Flow chart of literature review methodology.
    DownLoad: Full-Size Img PowerPoint

    Publication contribution analysis

    Table 1 presents the top 10 countries/regions, institutions, authors, and journals that published the most studies on Trichoderma formulations. As indicated in Table 1, China emerged as the country making the most significant contribution, with 1,231 publications, accounting for 20.33% of the total. India and Pakistan followed closely, ranking second and third, with 1,096 (18.10%) and 618 (10.20%) publications, respectively. Among the institutions, the Chinese Academy of Sciences held the top spot, boasting 160 (2.64%) publications. Following closely was the University of Agriculture, Faisalabad (144, 2.37%), and Nanjing Agricultural University (137, 2.26%). In the realm of scholarly contributions, prolific authors often set the tone for research trends. Identifying these influential scholars can shed light on the direction of the research field[29]. The leading author in the study of rhizosphere microorganisms was Wang Y, with 102 publications. Li Y, Zhang Y, and Hkan M were also highly prolific, each publishing nearly 90 studies. These works were predominantly featured in prominent journals in Ecology and Botany, such as Frontiers in Microbiology (3.73%), Frontiers in Plant Science (2.36%), and Plant and Soil (2.03%).

    Table 1.  Leading journals contributing to the existing body of knowledge in the field of formulation of Trichoderma.
    Sl. no. Name of journal No. of publication Citations
    1 Journal of Applied Microbiology 2 40
    2 Applied Microbiology and Biotechnology 2 16
    3 Indian Phytopathology 3 2
    4 Biological Control 2 59
    5 Crop Protection 2 30
    6 Frontiers in Microbiology 2 23
    7 Journal of Biological Control 2 1
    8 Medicinal Plants 2 5
     | Show Table
    DownLoad: CSV

    Scientific production

    The analysis of scientific production on Trichoderma formulations demonstrated the trend of publications per year on Trichoderma formulation studies. It was observed that published research showed a significant increase of 71.24% over the last decade (2016–2023) (Fig. 1). The increasing trend is possibly related to economic support from government programs, since funding for innovative, sustainable, and ecological research is being considered to meet the demand for food and mitigate environmental pollution[30]. Figure 2 illustrates a co-citation map of authors collaborating in the field of Trichoderma formulation. The purpose of conducting this co-citation analysis is to visually portray the knowledge base of the specific area of review. The analysis identifies three distinct clusters, each represented by different colored nodes: blue, red, and green. The green cluster stands out as it is associated with Harman, who has the highest collaboration, working with nine researchers on Trichoderma formulation research. The red cluster, on the other hand, signifies the second-highest collaboration, led by Mukherjee et al.[31] with six researchers. Lastly, the pink cluster represents the lowest level of collaboration among researchers, with only two researchers working together in this area.

    Figure 2.  Co-citation analysis of cited authors as the unit of analysis in the field of Trichoderma formulation.
    DownLoad: Full-Size Img PowerPoint

    Data analysis and findings

    Table 2 showcases the country–wise citation analysis, and the series presented here seems to have large variability in distribution. In terms of total citations of studies dedicated to Trichoderma formulations. Citations count of articles by country as a unit of analysis represents the popularity of a field of research in a particular region. India with 20 publications having 115 citations topped the list and, therefore, is the most impactful country contributing to the existing body of knowledge in the said domain followed by Italy with four publications having 69 citations and Brazil with three publications having 51 citations. From the viewpoint of the total number of publications, India holds first position, having 20 publications, followed by Italy having four publications.

    Table 2.  Leading countries contributing to the existing body of knowledge in the field of formulation of Trichoderma.
    Sl. no. Country No. of publication Citations
    1 Argentina 1 20
    2 Belgium 2 30
    3 Brazil 3 51
    4 China 2 82
    5 Croatia 1 30
    6 Finland 1 37
    7 India 20 115
    8 Italy 4 69
    9 New Zealand 2 21
    10 Portugal 1 67
    11 South korea 1 54
     | Show Table
    DownLoad: CSV

    The top researchers working in the field of Trichoderma formulation are presented in Table 2. The authors' citation count represents the recognition of their research work in a particular field of research. It is quite clear from the list of 13 author's citations that all the authors have at least 10 citations to their name based on the total citation count. Among the 13 authors Park et al.[32] has the highest number of citations of 57 followed by Herrera-Téllez et al.[33] having 47 and Hewedy et al.[34] having 44 citations. The analysis of bibliographic coupling in the Trichoderma formulation domain is represented in Fig. 3. This technique utilizes references from existing publications to elucidate the relevant literature[35]. For this study, five thematic clusters have been identified, labeled green, red, blue, yellow, and purple. Among these interconnected groups, India stands out as the country with the most extensive collaboration network, linked with 15 other countries. Given that India also holds the highest number of published documents (115), it was anticipated to be the central node in this cooperation network. The findings demonstrate the strong relationships between researchers and their respective institutional affiliations, emphasizing the scientific cooperation aimed at developing sustainable and ecologically sound strategies for crop protection in a competitive manner[36].

    Figure 3.  Bibliographic coupling of articles in the field of Trichoderma formulation.
    DownLoad: Full-Size Img PowerPoint

    In Fig. 4, a co-occurrence analysis of keywords with a minimum threshold of five occurrences is displayed. The network illustrates the most frequently utilized terms within the 'Trichoderma formulation' research domain, capturing the essence of the article's core content. The prevalence of these keywords can be indicative of the research direction and content within this specific field[37]. This analysis allows for the identification of developmental trends within a field and a comprehensive understanding of its current research status[38]. The co-occurrence graph of keywords reveals a total of four co-occurrence clusters (Fig. 4), encompassing themes like biocontrol, formulation, Trichoderma, and shelf life. Each cluster is further examined below, providing an in-depth portrayal of the prominent topics within the Trichoderma formulations landscape during the research period. Annual publication number leading years contributing to the existing body of knowledge in the field of formulation of Trichoderma is presented in Table 3.

    Figure 4.  Co-occurrence analysis based upon keywords from articles in the field of Trichoderma formulation.
    DownLoad: Full-Size Img PowerPoint
    Table 3.  Annual publication number leading years contributing to the existing body of knowledge in the field of formulation of Trichoderma.
    Sl. no. Year No. of publication
    1 2016 8
    2 2017 13
    3 2018 21
    4 2019 16
    5 2020 20
    6 2021 17
    7 2022 15
    8 2023 8
     | Show Table
    DownLoad: CSV

    The shift in annual publication counts serves as a vital benchmark for gauging the progress of a research field, lending insights into potential development trends[28]. Figure 4 provides a clear portrayal of the publication distribution in Trichoderma formulation from 2016 to 2023, illustrating a noticeable increase in annual article output. This surge suggests a heightened interest in the field over the past few years. Scientific research fields typically undergo a four-stage evolution[39] ; (1) the inception phase, characterized by the introduction of novel research areas or directions by notable scientists; (2) the expansion phase, where scientists gravitate toward the emerging research direction, leading to a proliferation of discussion topics; (3) the stabilization phase, marked by the amalgamation of new knowledge to form a distinct research context; and (4) the contraction phase, in which the number of new publications diminishes. Notably, the research on Trichoderma formulation seems to be currently in the expansion phase[40].

    Summary of review

    The publication pattern reveals a growing research interest in Trichoderma formulations, a relatively new field that is attracting increasing enthusiasm among scholars. Notably, the top contributors to this area, as identified through VOS viewer analysis, include key individuals, organizations, sources, and countries. Park emerges as the leading author based on citation count, followed by Herrera-Téllez and Hewedy. China, Portugal, Italy, and South Korea are recognized as major contributors to research in this field, as reflected in their citation counts. Conversely, India leads in terms of document count, demonstrating a significant contribution to the literature.

    Co-citation and bibliographic coupling analyses have identified three distinct thematic clusters. In the co-citation analysis, these clusters relate to application methods, types of Trichoderma formulations, and their biocontrol efficacy. Additionally, insights from the bibliometric analysis of biopesticide formulations have facilitated the integration of methods and strategies aimed at enhancing the effectiveness of Trichoderma formulations.

    Conclusions

    This paper conducts a bibliometric analysis to critically examine articles related to biological control, focusing specifically on those published in various indexed journals, and offers a comprehensive overview of the evolution of Trichoderma formulations over time. The primary objective of this research is to investigate and characterize the key literature on this topic, covering historical, current, and emerging developments in this dynamic field. Bibliometric techniques are employed to visualize the Trichoderma formulation landscape.

    To achieve this goal, the study analyses a dataset of articles obtained from the core collection databases of Scopus and Web of Science. Within the scope of this study, significant publications on Trichoderma formulations are meticulously reviewed to highlight the potential trajectory of Trichoderma's role in biological disease control in plants. The study identifies and examines the various developmental phases of Trichoderma formulations, offering a comprehensive analysis that can shape the future of this critical research area. Given the scarcity of comprehensive bibliometric studies on Trichoderma formulation research, this study seeks to fill this gap, making a significant contribution to the extensive readership interested in Trichoderma.

    Limitations and future research agenda

    This study has several limitations and challenges that must be considered by future researchers. First, the study relies on a single database, which could restrict the amount of available data. Additionally, the search criteria were limited to research articles, and only those with specific phrases in the title were included, which may not represent the complete dataset. However, Trichoderma's biological control mechanisms against plant fungal and nematode diseases involve various strategies, including competition, antibiosis, antagonism, and mycoparasitism. In addition to these, Trichoderma enhances plant growth and induces systemic resistance in plants, making it effective in controlling a wide range of plant fungal and nematode diseases[41]. Although biological control is effective, it generally requires time to become established in the environment, making it a slower process. Therefore, optimizing the formulation of Trichoderma-based products is essential to ensure their stability and efficacy. It is important to ensure that these formulations are compatible with other agricultural treatments, such as chemical fertilizers and pesticides, to maximize their overall effectiveness. Proper formulation can improve the shelf life, ease of application, and survival of Trichoderma under varying environmental conditions. Ongoing research is necessary to refine these formulations for broader application in integrated pest management programs[42]. This is a significant limitation as the analysis was restricted to articles published in journals, excluding other valuable sources like reviews, conferences, books, and book chapters. To overcome this limitation, future researchers should consider utilizing additional databases such as Scopus and Science Direct, which can provide more comprehensive data. This limitation may have impacted the study's ability to provide a comprehensive overview of the field.

    Author contributions

    The authors confirm contribution to the paper as follows: conceptualization: Kumar V, Mishra KK, Panda SR; writing − original draft preparation: Kumar V, Wagh AK, Mishra KK; writing − review and editing: Panda SR, Kumar V, Wagh AK; supervision: Kumar V, Panda SR, All authors have read and agreed to the published version of the manuscript.

    Data availability

    The data that support the findings of this study are available on request from the corresponding authors.

  • The authors declare that they have no conflict of interest.

  • Supplemental Table S1 Essential oil extraction data.
    Supplemental Table S2 Main components and relative contents of seven essential oils.
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  • Cite this article

    Liu H, Chen X, Chen H, Guo S, Huang C, et al. 2022. Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny. Ornamental Plant Research 2:7 doi: 10.48130/OPR-2022-0007
    Liu H, Chen X, Chen H, Guo S, Huang C, et al. 2022. Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny. Ornamental Plant Research 2:7 doi: 10.48130/OPR-2022-0007
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Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny

  • 1.

    Institute of Grassland, Flowers and Ecology, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center of Functional Floriculture, Beijing 100097, China

  • 2.

    College of Landscape Architecture, Sichuan Agricultural University, Chengdu 611130, China

  • 3.

    College of Landscape Architecture, Beijing University of Agriculture, Beijing 100097, China

  • 4.

    Chengdu Landscape Architecture Planning & Designing Institute, Chengdu Park City Research Center, Chengdu 610036, China

  • 5.

    Institute of Agri-food Processing and Nutrition (IAPN), Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China

  • Received: 23 November 2021
  • Accepted: 01 March 2022
  • Published online: 25 April 2022
Ornamental Plant Research  2,  Article number: 7  (2022)  |  Cite this article

Abstract: Chrysanthemum and Opisthopappus are genera that include perennial herbaceous floral species, including excellent varieties with strong fragrances resulting from long-term artificial selection. Thus, they are ornamentally and economically important flower resources. In this study, a water distillation method was used to extract essential oils from the inflorescences of Chrysanthemum and Opisthopappus wild resources and hybrid progeny with high essential oil contents (Chrysanthemum morifolium 'xiangjin', C. morifolium 'xiangyun', C. morifolium 'xinjiboju', Opisthopappus taihangensis, Opisthopappus longilobus, Chrysanthemum lavandulifolium, and C. morifolium 'minghuangju'). The essential oil extraction rates were as follows: 1.17‰, 2‰, 1.67‰, 2.17‰, 0.43‰, 1‰, and 1.17‰. On the basis of HS-SPME-GC-MS (Headspace solid phase microextraction-gas chromatography-mass spectrometry), 225 volatile compounds were detected in the seven analyzed essential oil samples. Each essential oil had a relative volatile component content exceeding 0.3. The three most abundant compounds were olefins (46 types), alcohols (34 types), and esters (18 types). The volatile components with relatively high contents included thymol, D-camphor, pinene, eucalyptol, 2-terpineol, terpineol, trans-caryophyllene, and β-elemene. These volatile compounds have strong biological activities and are useful components of medicines and daily-use products. An evaluation of their antibacterial effects demonstrated that the essential oils of C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, and C. 'minghuangju' inhibited the growth of Escherichia coli. The C. lavandulifolium essential oil inhibited the growth of Pectobacterium carotovorum. The results of this study will provide researchers with an important theoretical basis for the development and application of Chrysanthemum and Opisthopappus essential oils.

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    INTRODUCTION

    • Chrysanthemums are perennial floral species in the family Compositae[1]. They produce economically valuable ornamental flowers with multiple uses (e.g., as medicine, food, and tea)[2]. Opisthopappus Shih is a genus endemic to China and distributed in the Taihang Mountains. Opisthopappus taihangensis and Opisthopappus longilobus, which are the two species in this genus, are second-class, critically endangered, and protected plants in China[3]. Both species are resistant to drought, shade, and cold stresses. Their flowers are mostly white, making them an important germplasm resource with ecological, ornamental, and economic value[4−7].

      To date, research on Opisthopappus plants has mainly focused on the genetic differences and interrelationships among O. taihangensis varieties[8], the physiological characteristics underlying drought resistance and transcriptome changes[9,10], genetic diversity[11], tissue culture[3,12,13], metal element contents in the soil in which O. longilobus is grown[11], and hybrid breeding involving Opisthopappus plants and related species[14]. However, the fragrance and essential oil components of O. taihangensis and O. longilobus flowers have not been comprehensively identified and characterized. Therefore, the objective of this study was to detect and analyze the fragrance and essential oil components of Opisthopappus flowers, with a particular focus on their antibacterial properties, which may be relevant for increasing the economic value of Opisthopappus species. The findings of this study may provide researchers and breeders with important information related to the protection, development, and utility of endangered Opisthopappus plants.

      The commonly used methods for extracting essential oils include steam distillation, solvent extraction (including supercritical CO2 extraction), and the application of high pressure. Characteristic aromatic and volatile oils have been extracted from flowers, leaves, fruits, stems, and other plant parts. The main volatile components in essential oils are terpenes. The terpenoids of essential oils are primarily monoterpenes and sesquiterpenes. In addition to olefin, essential oils also contain alcohols, aldehydes, ketones, esters, and other naturally occurring terpenoids. The essential oils extracted from aromatic plants are an extremely important raw material in the fragrance industry and are widely exploited in the daily-use chemical industry. Essential oils are also used for the production of food and medicine because of their diverse biological activities[15,16]. The essential oils of chrysanthemum have various uses in many fields (e.g., to enhance the storage of vegetables and meat and food preservation). Unlike pesticides and other harmful compounds, chrysanthemum essential oils are natural and safe for human consumption. Moreover, they have antibacterial and antioxidant properties as well as proven pharmacological effects that can prevent infections[17−19], eliminate inflammation, and remove scars. Therefore, these essential oils have been used in cosmetics and for massage therapy[20]. The compounds in aromatic essential oils with the strongest antibacterial effects are mainly terpenes, phenols, and alcohols, which are commonly produced by aromatic plants[21]. Previous research revealed that aromatic plant essential oils inhibit the activities of pathogenic bacteria by altering the fatty acid outer membrane, degrading the cell membrane, and inducing the leakage of metabolites and ions[22]. Chrysanthemum indicum essential oils can be included in moisturizing creams, mosquito repellents, laundry detergents, dishwashing liquids, shower gels, and shampoos to provide these daily-use products with the fragrance and antibacterial and anti-inflammatory properties of C. indicum[23]. The predominant volatile aromatic components of the Chrysanthemum morifolium 'Tianmeng Mountain Imperial' essential oil include 22 types of hydrocarbons, 9 types of alcohols, 7 types of esters, and 2 types of ketones[24]. Researchers used a water distillation method to extract the essential oils of C. morifolium 'Kunlun Snow' plants. A micro-dilution method used to investigate the inhibitory effect of the C. morifolium 'Kunlun Snow' essential oil on cryptococcus fungi revealed that the essential oil treatment can degrade the fungal cell membrane and alter cell membrane permeability[25]. Other researchers extracted essential oils from C. morifolium 'Jiugongxiangju' stems and leaves via water distillation. The essential oils were analyzed by gas chromatography–mass spectrometry (GC-MS) and tested for their antibacterial properties. These analyses confirmed that C. morifolium 'Jiugongxiangju' essential oils have antibacterial effects[26]. Earlier research that applied GC-MS and GC-olfactometry techniques to identify the aromatic components in seven chrysanthemum essential oils revealed terpenes, esters, alcohols, ketones, acids, and aldehydes as the primary compounds[27]. Moreover, the antibacterial activities of the C. morifolium 'Chuju' essential oil and the underlying mechanism were determined on the basis of an SDS-PAGE analysis, an examination of DNA topoisomerase activity, and an oxidative respiration metabolism test. The results of the DNA topoisomerase analysis demonstrated that the C. morifolium 'Chuju' essential oil simultaneously inhibits the activities of topoisomerases I and II[28]. A previous investigation analyzed the essential oil components of three Chrysanthemum species (C. coronarium, C. fuscatum, and C. grandiflorum) by GC-MS, which revealed the insecticidal activities of the essential oils. Furthermore, essential oils extracted from various chrysanthemum species according to diverse methods can protect crops from pest infestations, with implications for small-scale grain production[29].

      On the basis of the available wild resource collection and the findings of our earlier hybridization research, we selected Chrysanthemum and Opisthopappus wild species, varieties, and hybrid offspring for this study. Essential oils were extracted from C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, C. lavandulifolium, and C. 'minghuangju' and their compositions were analyzed. Specifically, HS-SPME-GC-MS technology was used to identify the volatile components of the extracted essential oils and to analyze the types of compounds and the components unique to particular plants. The results of this study may be relevant for characterizing chrysanthemum essential oil components with important industrial uses.

    RESULTS

      Extraction of essential oils

    • We previously collected wild resources of O. taihangensis, O. longilobus, and C. lavandulifolium as well as the hybrid offspring of C. lavandulifolium (i.e., C. 'xiangjin' and C. 'xiangyun'). We also collected C. 'xinjiboju' and C. 'minghuangju' plants, which produce flowers with a special aroma suitable for tea (Fig. 1). Regarding the hybrids and wild species with high essential oil contents, relatively large amounts of essential oils have been extracted from the inflorescences of C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, C. lavandulifolium, and C. 'minghuangju'. The test materials were obtained from the Shunyi Beilangzhong Experimental Base of the Beijing Academy of Agriculture and Forestry Sciences. By using a water distillation method, we extracted differentially colored essential oils from the seven analyzed samples (Fig. 2). A further analysis revealed the essential oils of C. 'xiangyun' and O. longilobus were bright blue and black, respectively. The essential oil extraction rate was highest for O. taihangensis (2.17‰), followed by C. 'xiangyun' (2‰) and C. 'xinjiboju' (1.67‰) (Supplemental Table S1, Fig. 3).

      Figure 1. 

      Plant material used in the extraction of essential oil (a) C. 'xiangjin' flowers and leaves; (b) C. 'xiangyun' flowers and leaves; (c) C. lavandulifolium flowers and leaves; (d) C. 'xinjiboju' flower and leaves; (e) O. taihangensis flowers and leaves; (f) O. longilobus flower and leaves; (g) C. 'minghuangju' flower and leaves.

      Figure 2. 

      Appearance of the essential oils extracted from the seven examined materials. (a) C. 'xiangyun'; (b) O. taihangensis; (c) C. 'minghuangju'; (d) C. 'xiangjin'; (e) O. longilobus; (f) C. 'xinjiboju'; (g) C. lavandulifolium.

      Figure 3. 

      Extraction rate of various essential oils.

      Analysis of the volatile components of essential oils

    • By analyzing the components of the seven essential oils, a total of 225 compounds were identified and quantified. More specifically, 60 olefins (including enones and enols), 34 alcohols, 18 esters, 8 alkanes, 3 types of ketones, and 2 types of aromatic compounds were detected as the main volatile components.

      The volatile components of the essential oil extracted from C. 'xiangjin' were separated and identified by GC-MS. A total of 62 aromatic compounds were detected; the ion current diagram is presented in Fig. 4a. The analysis of the volatile components of the C. 'xiangjin' essential oil (Supplemental Table S2) identified bicyclo[3.1.0]hex-3-en-2-one, 4-methyl-1-(1-methylethyl)- (24.62%), bicyclo[3.1.1]hept-2-en-4-ol, 2,6,6-trimethyl-, acetate (17.7%), and thymol (11.06%) as three highly abundant components.

      Figure 4. 

      Ion flow diagram of essential oil of 7 plant materials. (a) Ion current diagram of the C. 'xiangjin' essential oil. I: Bicyclo[3.1.0]hex-3-en-2-one, 4-methyl-1-(1-methylethyl)-; II: Bicyclo[3.1.1]hept-2-en-4-ol, 2,6,6-trimethyl-, acetate; III: Thymol. (b) Ion current diagram of the C. 'xiangyun' essential oil. I: Bicyclo[2.2.1]heptan-2-one, 1,7,7-trimethyl-, (1R)-. (c) Ion current diagram of the C. 'xinjiboju' essential oil. I: Bicyclo(3.3.1)non-2-ene; II: Bicyclo[3.1.1]hept-2-en-6-one, 2,7,7-trimethyl-; III: Bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)-. (d) Ion current diagram of the O. taihangensis essential oil. I: Bicyclo[3.1.0]hexan-3-one, 4-methyl-1-(1-methylethyl)-, [1S-(1.alpha.,4.beta.,5.alpha.)]-. (e) Ion current diagram of the O. longilobus essential oil. I: Eucalyptol. (f) Ion current diagram of the C. lavandulifolium essential oil. I: Eucalyptol; II: 2H-Pyran-3(4H)-one, 6-ethenyldihydro-2,2,6-trimethyl-; III: Bicyclo[2.2.1]heptan-2-one, 1,7,7-trimethyl-, (1R)-. (g) Ion current diagram of the C. 'minghuangju' essential oil. I: Bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)-; II: Cyclohexane, 1-ethenyl-1-methyl-2,4-bis(1-methylethenyl)-, [1S-(1.alpha.,2.beta.,4.beta.)]-; III: Agarospirol.

      The extracted volatile components of the C. 'xiangyun' essential oil were separated and identified by GC-MS. A total of 56 aromatic compounds were detected. The ion current diagram is presented in Fig. 4b, whereas the results of the analysis of the volatile components are provided in Supplemental Table S2. According to the data, D-camphor (bicyclo[2.2.1]heptan-2-one, 1,7,7-trimethyl-, (1R)-) (47.06%) was the component with the highest relative content in the C. 'xiangyun' essential oil.

      The separation and identification of the volatile components of the C. 'xinjiboju' essential oil by GC-MS resulted in the detection of 64 aromatic compounds. The ion current diagram and the results of the analysis of the volatile components are presented in Fig. 4c and Supplemental Table S2, respectively. The data revealed the relatively high contents of pinene ((1R)-2,6,6-trimethylbicyclo[3.1.1]hept-2-ene) (3.38%), eucalyptol (5.72%), bicyclo(3.3.1)non-2-ene (10.025%), bicyclo[3.1.1]hept-2-ene-6-one, 2,7,7-trimethyl- (12.48%), and bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)- (10.36%).

      The GC-MS analysis of the volatile components of the O. taihangensis essential oil detected 71 aromatic compounds. The ion current diagram is presented in Fig. 4d, whereas the results of the analysis of the volatile components are provided in Supplemental Table S2. The data indicated eucalyptol (5.74%), linalool (1,6-octadien-3-ol, 3,7-dimethyl-) (7.73%), bicyclo[3.1.0]hexan-3-one, 4-methyl-1-(1-methylethyl)-, [1S-(1α,4β,5α)]- (15.26%), thujone (8.38%), and 2-naphthalenemethanol, decahydro-.alpha.,.alpha.,4a-trimethyl-8-methylene-, [2R-(2.alpha.,4a.alpha.,8a.beta.)]- (7.41%) were highly abundant in the O. taihangensis essential oil.

      The volatile components in the O. longilobus essential oil were separated and identified by GC-MS, resulting in the detection of 66 aromatic compounds. The ion current diagram is presented in Fig. 4e. The results of the analysis of the volatile components are listed in Supplemental Table S2. The O. longilobus essential oil contained relatively large amounts of (1R)-(+)-α-pinene (9.06%) and eucalyptol (27.71%).

      On the basis of the GC-MS analysis of the volatile components of the essential oil extracted from C. lavandulifolium, 74 aromatic compounds were detected. The ion current diagram and the results of the analysis of the volatile components are respectively presented in Fig. 4f and Supplemental Table S2. The data reflected the relatively high contents of eucalyptol (5.06%), 2H-pyran-3(4H)-one, 6-ethenyldihydro-2,2,6-trimethyl- (9.36%), and D-camphor (16.39%).

      The volatile components in the C. 'minghuangju' essential oil separated and identified by GC-MS included 63 aromatic compounds. The ion current diagram is presented in Fig. 4g and the results of the analysis of the volatile components are provided in Supplemental Table S2. The data revealed the relatively high contents of (1R)-2,6,6-trimethylbicyclo[3.1.1]hept-2-ene (3.28%), .beta.-phellandrene (4.55%), eucalyptol (8.02%), D(+)-camphor (7.58%), bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)- (11.63%), 3-cyclohexen-1-ol, 4-methyl-1-(1-methylethyl)- (4.44%), bornyl acetate (4.4%), cyclohexane, 1-ethenyl-1-methyl-2,4-bis(1-methylethenyl)-, [1S-(1.alpha.,2.beta.,4.beta.)]- (10.14%), 3-decanynoic acid (3.99%), and agarospirol (9.12%).

      Comparison and analysis of the volatile components of several chrysanthemum essential oils

    • The three components that were relatively highly abundant in the C. 'xiangjin' essential oil were bicyclo[3.1.0]hex-3-en-2-one, 4-methyl-1-(1-methylethyl)- (24.62%), bicyclo[3.1.1]hept-2-en-4-ol, 2,6,6-trimethyl-, acetate (17.7%), and thymol (11.06%). The volatile component with the highest relative content in the C. 'xiangyun' essential oil was bicyclo[2.2.1]heptan-2-one, 1,7,7-trimethyl-, (1R)- (47.06%). The components with the highest relative contents in the C. 'xinjiboju' essential oil were (1R)-2,6,6-trimethylbicyclo[3.1.1]hept-2-ene (3.38%), eucalyptol (5.72%), bicyclo(3.3.1)non-2-ene (10.025%), bicyclo[3.1.1]hept-2-en-6-one, 2,7,7-trimethyl- (12.48%), and bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)- (10.36%). The components with the highest relative contents in the O. taihangensis essential oil were eucalyptol (5.74%), 1,6-octadien-3-ol, 3,7-dimethyl- (7.73%), bicyclo[3.1.0]hexan-3-one, 4-methyl-1-(1-methylethyl)-, [1S-(1.alpha.,4.beta.,5.alpha.)]- (15.26%), thujone (8.38%), and 2-naphthalenemethanol, decahydro-.alpha.,.alpha.,4a-trimethyl-8-methylene-, [2R-(2.alpha.,4a.alpha.,8a.beta.)]- (7.41%). The components with the highest relative contents in the O. longilobus essential oil were (1R)-2,6,6-trimethylbicyclo[3.1.1]hept-2-ene (9.06%) and eucalyptol (27.71%). The components with the highest relative contents in the C. lavandulifolium essential oil were eucalyptol (5.06%), 2H-pyran-3(4H)-one, 6-ethenyldihydro-2,2,6-trimethyl- (9.36%), and bicyclo[2.2.1]heptan-2-one, 1,7,7-trimethyl-, (1R)- (16.39%). The components with the highest relative contents in the C. 'minghuangju' essential oil were (1R)-2,6,6-trimethylbicyclo[3.1.1]hept-2-ene (3.28%), .beta.-phellandrene (4.55%), eucalyptol (8.02%), D(+)-camphor (7.58%), bicyclo[2.2.1]heptan-2-ol, 1,7,7-trimethyl-, (1S-endo)- (11.63%), 3-cyclohexen-1-ol, 4-methyl-1-(1-methylethyl)- (4.44%), bornyl acetate (4.4%), cyclohexane, 1-ethenyl-1-methyl-2,4-bis(1-methylethenyl)-, [1S-(1.alpha.,2.beta.,4.beta.)]- (10.14%), 3-decanynoic acid (3.99%), and agarospirol (9.12%).

      A total of 133 aromatic compounds were detected during the comparison of the C. 'xiangjin', C. 'xiangyun', and C. lavandulifolium (wild species) essential oils (Fig. 5a). The following 15 components were common among the three essential oils (11.3% of the total components): pinene; β-phellandrene; β-myrcene; α-phellandrene; o-cumene; γ-terpinene; cis-4-carene; bicyclo[3.1.1]hept-2-ene-6-one, 2,7,7-trimethyl-; (S)-cis-verbenol; isocyclocitral; bicyclo[2.2.1]heptan-3-one, 6,6-dimethyl-2-methylene-; bicyclo[3.1.1]hept-2-en-4-ol, 2,6,6-trimethyl-, acetic acid; myrtyl acetate; caryophyllin; and farnesene.

      Figure 5. 

      Comparison of the essential oil components. (a) C. 'xiangjin', C. 'xiangyun', and C. lavandulifolium essential oil comparison group; (b) C. 'minghuangju', C. lavandulifolium, and C. 'xinjiboju' essential oil comparison group; (c) O. taihangensis and O. longilobus essential oil comparison group.

      Regarding the comparison of the essential oils of three wild chrysanthemums (C. 'minghuangju', C. lavandulifolium, and C. 'xinjiboju'), a total of 152 aromatic compounds were detected, of which 15 were common to all three essential oils (9.9% of the total components) (Fig. 5b). The analysis of the essential oil contents indicated the aromatic compounds were most similar between the C. lavandulifolium and C. 'xinjiboju' essential oils.

      The comparison of the essential oils extracted from the endangered O. taihangensis and O. longilobus samples detected 137 aromatic compounds, including 29 compounds that were present in both essential oils (26.9% of the total components) (Fig. 5c).

      Verification of the antibacterial effects of chrysanthemum essential oils

    • The antibacterial effects of the essential oils extracted from C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, C. lavandulifolium, and C. 'minghuangju' were tested using Escherichia coli DH5α and Pectobacterium carotovorum strain BC1, which are difficult to control. After a 24-h incubation at 37 °C, an examination of the E. coli cultures on solid medium in plates revealed growth inhibition zones for the C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, and C. 'minghuangju' essential oil treatments. In contrast, there was no growth inhibition zone for the control treatment. The C. lavandulifolium essential oil treatment clearly inhibited P. carotovorum growth, in contrast to the lack of inhibition for the control treatment. Of the seven analyzed essential oils, those of C. 'xiangyun', C. 'xinjiboju', O. taihangensis, and C. lavandulifolium had the strongest antibacterial effects (Table 1, Fig. 6).

      Table 1.  Antibacterial effects of seven essential oils.

      Essential oil type nameBacteriostatic
      ring width (mm)      		The average
      value (mm)
      C. 'xiangjin' essential oil3.252.2532.8 ± 0.55
      C. 'xiangyun' essential oil104.2587.42 ± 3.17
      C. 'xinjiboju' essential oil3.254.25116.17 ± 4.84
      O. taihangensis essential oil3.45141511.15 ± 7.7
      O. longilobus essential oil2.352.1522.17 ± 0.18
      C. 'minghuangju' essential oil2.552.2532.6 ± 0.4
      C. lavandulifolium essential oil4.253.754.504.17 ± 0.52

      Figure 6. 

      Antibacterial effects of the essential oils. 1–3: C. 'xiangyun' essential oil; 4–6: C. 'xinjiboju' essential oil; 7–9: C. 'xiangjin' essential oil; 10–12: O. taihangensis essential oil; 13–15: O. longilobus essential oil; 16–18: C. 'minghuangju' essential oil; 19–21: C. lavandulifolium essential oil; 22–24: E. coli DH5α control; 25–27: P. carotovorum control.

    DISCUSSION

    • The most common chrysanthemum essential oil is yellow or green, In this study, the C. 'xiangyun' and C. 'minghuangju' essential oils were extracted at a relatively high rate and had a special color. Essential oils vary significantly in terms of color because of the diversity in their phytochemical components (e.g., ochre red myrrh essential oil, red orange essential oil with blue–purple fluorescence under high-intensity light, blue chamomile essential oil, black vetiver essential oil, and light green fragrant bergamot essential oil). The essential oil of Matricaria recutita, which belongs to the family Compositae, is similar to the C. 'xiangyun' and C. 'minghuangju' essential oils extracted in this study, both of which were blue. The chamomile essential oil is blue because of the presence of the organic compound azulene. The chamomile plant itself does not contain azulene, but it does contain a matricin. The matricin is the result of a series of chemical reactions (e.g., dehydration, hydrolysis, and decarboxylation) during the extraction process. The matricin are responsible for the blue coloration of the chamomile essential oil. Naturally obtained azulene may produce a variety of colors, including blue, green, blue–purple, or even red–purple. In addition to German chamomile, some yarrow plants also contain matricin. Thus, their essential oil also appears blue because of the presence of the azure hydrocarbon. Moreover, some mugwort plants, such as wormwood, also produce blue essential oils.

      Regarding the essential oil odors, we revealed that the 225 compounds detected in seven essential oil samples included caryophyllene (trans-caryophyllene), o-cumene, γ-terpinene, (1S, 3R)-cis-4-carene, β-phellandrene, and α-phellandrene. The relatively abundant compounds included thymol, D-camphor, eucalyptol, borneol, linalool, syringone, (−)-α-cubic benzene, α-epoxy-terpineol acetate, pinene, β-phellandrene, 4-terpene alcohol, borneol acetate, beta-elemene, 3-decenoic acid, and linalool, of which pinene, D-camphor, and eucalyptol were the main essential oil constituents with a pleasant aroma as well as biological activities.

      Among the identified compounds, the representative acyclic monoterpenes were myrcene, linalool, and phellandrene; the representative monocyclic monoterpenes were terpineol and terpinene; the representative bicyclic monoterpenes were pinene, camphene alkene, and camphor; and the representative sesquiterpenes were farnesol and caryophyllene. Small aliphatic compounds, including alcohols, aldehydes, ketones, and acids, were also frequently detected in the analyzed essential oils.

      Among them, caryophyllene, camphor and other substances are generally the main volatile components of wild chrysanthemum, ground cover chrysanthemum and some wormwood plants[29,30]. Both camphor and camphene have camphor-type aromas, so the odor of O. longilobus, C. 'xiangyun' and C. lavandulifolium essential oil with relatively high contents of camphor and camphene are relatively cool and slightly irritating. The highest relative content in O. longilobus essential oil is Eucalyptol. Eucalyptol is a monoterpenoid compound with a camphor-like odor.

      Linalool, which was identified as a component of the Taihang chrysanthemum essential oil, produces an aroma that is similar to that of lily of the valley and is one of the most important compounds in the fragrance and flavor industries. Additionally, it decreases the pain responses mediated by various neurotransmitter systems[31] and has antioxidant, anti-inflammatory, anticancer, antispasmodic, and antiparasitic activities[32]. However, a previous study indicated that more than 95% of the linalool produced worldwide is used as an aromatizer and flavor enhancer[33]. Plants with high linalool contents include oregano (90.3%), coriander (73.7%), salvia (70.6%), spinach (61.5%), basil (43.1%), prickly ash (46.1%), and marjoram (41.2%)[34]. The total annual demand for L-linalool is 12,000 tons, but only 5,400 tons are produced worldwide under natural conditions.

      Camphor, which was detected as the most abundant component in the C. 'xiangyun' essential oil, has a distinctive spicy aroma and taste, although its taste eventually dissipates. Moreover, camphor has a strong inhibitory effect on pests and bacteria. Specifically, it inhibits E. coli growth because of its detrimental effects on bacterial metabolism, chemotaxis, and anti-stress-related responses[35].

      Eucalyptol, which has the highest relative content in O. longilobus essential oil, is anti-inflammatory and analgesic, reducing pain and inflammation through mechanisms that may involve antioxidant effects[36].

      Beta-phellandrene is a common constituent of aromatic plant essential oils. It is a natural bioactive insecticide[37]. Many bioinsecticides contain β-phellandrene as an important active ingredient[38]. Caryophyllene is a bicyclic sesquiterpenoid that can be used to alter the flavor of foods containing clove, nutmeg, and citrus components[39]. Furthermore, γ-terpinene and α-terpinene often coexist and are associated with citrus aromas[40]. Phellandrene is a spice intermediate that is also associated with citrus aromas. It is commonly used as a natural active ingredient in biopesticides. It can also be used as a synthetic raw material for the production of terpene resins and menthol. The antibacterial, antiseptic, and insecticidal components of chrysanthemum essential oils, including β-thumberene, β-phellandrene, and other volatile compounds, are irritating to the skin. Thus, chrysanthemum essential oils should be diluted with other essential oils before they are used.

      Essential oils produced by aromatic plants have a variety of functions. For example, most of the compounds that are responsible for the volatilized odors of essential oils also have strong antibacterial effects. Furthermore, in addition to inhibiting the growth of bacteria and fungi, the volatile compounds in essential oils can attract insect pollinators, prevent pest infestations, and inhibit the growth of other plants (i.e., allelopathic effect). As pure natural bacteriostatic agents, plant essential oils leave minimal residues and are volatile, highly degradable, and relatively non-toxic (i.e., environmentally friendly), which is in sharp contrast to many synthetic pesticides and insecticides. Therefore, they have been included in horticultural products, food, medicine, and beauty products. They are also currently the focus of considerable research and development across industries. In this study, we extracted chrysanthemum essential oils and verified their antibacterial effects.

    MATERIALS AND METHODS

      Plant materials

    • The experimental materials (C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, C. lavandulifolium, and C. 'minghuangju') were collected from the Shunyi Beilangzhong Experimental Base of the Beijing Academy of Agriculture and Forestry Sciences (Beijing, China).

      Extraction of essential oils

    • All water distillers used for extracting essential oils were 10-L desktop essential oil pure water distillers (Luosha Biological Company China, Jiangsu). The collected fresh plant samples were weighed and then added to the distillers. The fresh plant sample weights were as follows: C. 'xiangjin': 3,000 g; C. 'xiangyun': 1,060 g; C. 'xinjiboju': 3,000 g; O. taihangensis: 3,000 g; O. longilobus: 2,300 g; C. lavandulifolium: 3,000 g; and C. 'minghuangju': 3,000 g. After adding 6 L deionized water, an electric ceramic stove was used to heat the solution (2,000 W) to boiling, after which the stove was adjusted to 1,200 W and the condensed water supply was turned on for a 2-h distillation. The essential oil content after the extraction was recorded and then the essential oil extraction rate was calculated as follows: essential oil extraction rate (‰) = essential oil weight/material sample weight × 1,000. Additionally, the state of the essential oils was examined. Upon completion of the distillation, the distillate was collected and the pure dew was removed to obtain the essential oil with a strong fragrance at −4 °C and in darkness. The volatile components of the essential oils extracted by water distillation were subsequently analyzed.

      Analysis of the volatile components in the essential oils

    • The Shimadzu GCMS-QP2010 system was used to detect and analyze the essential oils from C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, C. lavandulifolium, and C. 'minghuangju'. The volatile compounds in the essential oils were detected and analyzed by HS-SPME-GC-MS. The chromatographic column was a DB-5MS quartz capillary column (30 m × 0.25 mm × 0.25 µm). The carrier gas was He (99.999%) and the injection port temperature was 250 °C. Additionally, the split injection mode was used, with a total flow rate of 17.1 ml/min. The split ratio was 10, the ion source temperature was 200 °C, and the interface temperature was 250 °C. The MS analysis was completed using a detector at 1 kV and a mass scan range of 30–500 m/z in the full scan mode. The heating program was 30 min long, with an initial temperature of 50 °C, which was maintained for 2 min, after which it was increased to 220 °C at 8 °C/min and then maintained for 6.75 min. The solvent cut time was 3 min. The solid phase extraction was performed using a 50/30 µm DVB/CAR PDMS fiber. The sample was added to a 15-ml glass bottle and then placed in a water bath at 50 °C. The fiber was inserted into the headspace for a 30-min extraction. The extract was desorbed in the injection port at 250 °C for 3 min.

      Essential oil samples were collected after adding 5 µl methanol to 995 µl formulated oil. The resulting 1-ml solution was diluted 10-fold and then added to a 5-µl sample collected from the headspace of the 15-ml glass bottle.

      Verification of the antibacterial properties of the essential oils

    • The standard strains of E. coli (DH5α) and P. carotovorum (BC1) were used to assess the antibacterial effects of the essential oils. Specifically, bacterial cultures (1 × 108 CFU/ml) with no antibiotics were uniformly applied on solid LB medium in plates. A 100-µl aliquot of each essential oil was added to a small hole (1 cm diameter) in the middle of the plates. More specifically, the extracted essential oils of C. 'xiangjin', C. 'xiangyun', C. 'xinjiboju', O. taihangensis, O. longilobus, and C. 'minghuangju' were added to the plates with E. coli (DH5α), whereas the essential oil of C. lavandulifolium was added to the plates with P. carotovorum (BC1). Additionally, the plates with no essential oil added to the hole were used as the controls. After a 24-h incubation at 37 °C, the bacterial growth on each plate was examined.

      Acknowledgments

      • We thank Liwen Bianji (Edanz) (www.liwenbianji.cn) for editing the English text of a draft of this manuscript. This research was supported by the National Natural Science Foundation of China (31901354), the Innovation Foundation of the Beijing Academy of Agriculture and Forestry Sciences (KJCX20200112), and the Science and Technology Innovation Capacity Construction Project of the Beijing Academy of Agriculture and Forestry Sciences (KJCX20200113-30 and KJCX20200302-03).

      Conflict of interest

      • The authors declare that they have no conflict of interest.

      • # These authors contributed equally: Hua Liu, Xiaoxi Chen

      Supplementary information
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      • Copyright: © 2022 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (6)  Table (1) References (40)
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    Liu H, Chen X, Chen H, Guo S, Huang C, et al. 2022. Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny. Ornamental Plant Research 2:7 doi: 10.48130/OPR-2022-0007
    Liu H, Chen X, Chen H, Guo S, Huang C, et al. 2022. Detection and analysis of the volatile components in the essential oils of Chrysanthemum and Opisthopappus species and their hybrid progeny. Ornamental Plant Research 2:7 doi: 10.48130/OPR-2022-0007
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  • Introduction
  • Results

  • Extraction of essential oils

  • Analysis of the volatile components of essential oils

  • Comparison and analysis of the volatile components of several chrysanthemum essential oils

  • Verification of the antibacterial effects of chrysanthemum essential oils

  • Discussion
  • Materials and methods

  • Plant materials

  • Extraction of essential oils

  • Analysis of the volatile components in the essential oils

  • Verification of the antibacterial properties of the essential oils

  • Acknowledgments
  • Conflict of interest
  • Supplementary information
  • Rights and permissions
  • About this article
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