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Effects of Rhizosphere Fungi on the Chemical Composition of Fruits of The Chen et al. BMC Microbiology (2021) 21:206 https://doi.org/10.1186/s12866-021-02216-z RESEARCH ARTICLE Open Access Effects of rhizosphere fungi on the chemical composition of fruits of the medicinal plant Cinnamomum migao endemic to southwestern China Jingzhong Chen1, Xiaolong Huang1, Bingli Tong1, Deng Wang1, Jiming Liu1*, Xiaofeng Liao2 and Qingwen Sun3 Abstract Background: This study examined how rhizosphere fungi influence the accumulation of chemical components in fruits of a small population species of Cinnamomum migao. Results: Ascomycota and Basidiomycota were dominant in the rhizosphere fungal community of C. migao. Pestalotiopsis and Gibellulopsis were associated with α-Terpineol and sabinene content, and Gibellulopsis was associated with crude fat and carbohydrate content. There were significant differences in rhizosphere fungal populations between watersheds, and there was no obvious change between fruiting periods. Gibberella, Ilyonectria, Micropsalliota, and Geminibasidium promoted sabinene accumulation, and Clitocybula promoted α-Terpineol accumulation. Conclusion: The climate-related differentiation of rhizosphere fungal communities in watershed areas is the main driver of the chemical composition of C. migao fruit. The control of the production of biologically active compounds by the rhizosphere fungal community provides new opportunities to increase the industrial and medicinal value of the fruit of C. migao. Keywords: Cinnamomum migao, Small watershed, Fruit period, Rhizosphere fungi, Chemical components Background organic compounds secreted by plant roots provide en- The rhizosphere represents the interface of plant-soil in- ergy for and induce greater densities of rhizosphere teractions and was first proposed by Hiltner in 1904. fungi [50]. Under natural conditions, rhizosphere fungi The rhizosphere includes the microenvironment 0 ~ 2 form a beneficial symbiotic relationship with most mm between the root surface and soil [24] and repre- plants, the rhizosphere fungal providing nitrogen and sents the node of energy exchange between plant and phosphorus in return for their hosts, and can signifi- soil. Interactions in the rhizosphere alter the physical, cantly promote the utilization efficiency of soil nutrients chemical, and biological characteristics of the soil [31]. by plants [53]. The influence of rhizosphere fungi on The diversity and function of rhizosphere fungi are often plant growth and development has been widely studied, related to root exudates (proteins and sugars), and many particularly in the context of improving plant productiv- ity and crop yields [51]. Many studies have shown the influence of rhizosphere fungi on the chemical compos- * Correspondence: [email protected] ition of medicinal plants [11, 77]. Indeed, fungal com- 1Forest Ecology Research Center, College of Forestry, Guizhou University, Guiyang 550025, Guihzou Province, China munities in the rhizosphere promote the accumulation Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Chen et al. BMC Microbiology (2021) 21:206 Page 2 of 14 of beneficial substances in medicinal parts, with some In order to explore the influence of special rhizosphere fungi directly secreting plant growth hormones or other fungal communities on the chemical composition of C. important metabolites [4, 27, 32]. migao in a small watershed climate, we studied the dis- C. migao is a large evergreen of the Lauraceae family tribution of C. migao in small watersheds (Yujiang, Pan- and is endemic in southwest China. It is only distributed jiang, and Hongshui Rivers) and different fruiting in the dry and hot valleys formed by the Yujiang, Pan- periods (young fruit period, closed immature period, ma- jiang, and Hongshui Rivers at the border of the prov- turity period). We also explored changes in the rhizo- inces of southwestern Yunnan, Guizhou, and Guangxi sphere fungal community and the relationship between [39]. C. migao fruit is rich in metabolites such as sugar, the climate of the small watershed and the chemical crude fat, and volatile oils [69, 78]. Among the Miao and properties of the rhizosphere soil. We used high- Zhuang populations in southwestern China, C. migao throughput sequencing to characterize the fungal com- fruit is used as a seasoning and as traditional herbal munities and measured the dynamic changes in the medicine [76]. Pharmacological studies have shown that chemical composition of C. migao fruit. The results C. migao fruit effectively treats gastrointestinal tract and showed that the rhizosphere fungi affected the C. migao cardiovascular diseases [38, 70, 71, 74]. Indeed, four pa- fruit content of carbohydrate, crude fat, α-terpineol, and tent medicines in China contain C. migao fruit as the sabinene. The fungal communities significantly differed main ingredient and have achieved sales of hundreds of between watershed areas but not between fruiting pe- millions of RMB. C. migao fruit is only distributed in the riods. We observed correlations and dynamic models narrow region on the borders of the Panjiang, Yujiang, that explain to a certain extent that the microclimate- and Hongshui Rivers with an area of about 160,000 km2 dependent rhizosphere fungal community may be the in southwestern China and is cataloged in the List of Red cause of the geographic variation in the chemical com- Species of Biodiversity in China-Volume of Higher Plants position of the fruit. These findings provide a feasible as near-endangered [47]. Studies have confirmed the strategy for improving the medicinal value of the fruit of considerable geographical variation in the chemical com- C. migao by controlling the rhizosphere microbiome. position of C. migao fruit despite the narrow regional distribution, and the variety is not genetically derived. Results Researchers have suggested that the chemical compo- Alpha diversity and fungal composition of rhizosphere nents of C. migao fruit may be closely related to the cli- soil fungi mate of the small watershed in the plant’s distribution The fungal communities included Ascomycota, Basidio- region [9, 79]. Karst landforms characterize the geog- mycota, and Zygomycota (Fig. 1a). The Zygomycota raphy of southwest China; this special geomorphic dis- (37.99%) was most abundant in the Yujiang River, continuity has formed many small watersheds with followed by Basidiomycota (35.14%). The Ascomycota different climates [19]. The climate differences formed (38.11%) and Basidiomycota (33.24%) were most abun- by this special geographic area also promoted species dant in the Hengshui River. The Basidiomycota (38.15%) differentiation and rich species diversity, including the group is the most abundant, followed by Ascomycota ecological differentiation of fungal populations to form (25.14%) in the Panjiang River. In different fruiting pe- special ecologically functional populations [42, 62]. Ex- riods, the Ascomycota, Basidiomycota,andMortierello- tensive studies confirmed that environmental differences mycota were the main groups. Ascomycota was the most affect the feedback mechanism between plants and abundant (48.70% in the young fruit period, 34.96% in rhizosphere fungi, which then influence plant growth the closed immature period, and 34.66% in the mature and chemical characteristics [37, 54, 70, 71]. We aimed period), followed by Basidiomycota (14.47% in the young to understand how climatic differences between small fruit period, 26.07% in the closed immature period, watersheds affect the composition and function of the 23.43% in the mature period) (Fig. 1b). All samples con- rhizosphere fungal community of C. migao and the tained a large number of unidentified fungal groups, and chemical composition of the fruit. This study was con- it may be necessary to strengthen the sequencing depth ducted with the aim of answering the following research in order to identify them. A total of 2,059,189 sequences questions: How do environmental differences in small were obtained from the soil samples, which were divided watersheds and different fruiting periods affect the com- into 2112 OTUs. The OTU and Shannon index dilution position and function of the fungal community in the curves of each sample gradually flattened (Figure S1). rhizosphere of C. migao? How do differences in the The quantity can reflect the vast majority of microbial community composition and function of C. migao rhizo- diversity information in the sample. The student t-test sphere fungi
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