Diversity and function of rhizosphere microorganisms in medicinal plant Polygonatum cyrtonema Hua

Diversity and function of rhizosphere microorganisms in medicinal plant Polygonatum cyrtonema Hua | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 9 March 2024 V1 Latest version Share on Diversity and function of rhizosphere microorganisms in medicinal plant Polygonatum cyrtonema Hua Authors : Liu Haiyan , Sun Yingying , Hou Jing , and zhou duan 0009-0000-3203-4182 [email protected] Authors Info & Affiliations https://doi.org/10.22541/au.170995964.42772955/v1 303 views 188 downloads Contents Abstract Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract In China, Polygonatum cyrtonema Hua (Huangjing) is known for its medicinal and edible properties. Multiple environmental factors can shape plant-microbiome interactions. The cultivated sample sites were enriched characteristic fungi by Clonostachys divergens and Archaeorhizomycetes spp. whereas wild sample sites were enriched particular by Geminibasidium spp. and Bifiguratus spp. The number of observed species was lower in cultivated soil samples compared with wild ones by alpha diversity analysis. Functional annotation showed that the xylanolysis metabolism pathway was more abundant in rhizosphere microorganisms of cultivated P. cyrtonema Hua. The co-occurrence network showed positively interacted between Mucoromycota and Rozellomycota in the cultivated rhizosphere soil. Moreover, this result indicated that biomass of cultivated plant was significantly greater than that of the wild samples, and the polysaccharide content of the cultivated rhizomes was higher. In this study, we may predict basic and potential microbes that beneficial for the P. cyrtonema Hua rhizosphere improve the productivity and quality. Introduction Polygonatum cyrtonema Hua is a well-known traditional Chinese medicine for the treatment of upset stomachs, lung diseases, and diabetes that widely distributed in south China (Zhao et al., 2018; Xie et al., 2023). Polygonatum rhizomes are commonly cultivated for reproduction and are often widely used as functional foods and ornamental plants (Zhao et al., 2018). With the increasing demand for rhizomes, wild P. cyrtonema Hua medicinal plants have been over-collected, causing an acute shortage (Zhang et al., 2021). Currently, the annual demand for Polygonatum is up to 4000 tons in China. Thus, cultivation techniques have been used to meet the increasing market demand for Polygonatum rhizomes (Zhang et al., 2021; Tian et al., 2021). Most Polygonatum plants grow in moist and shady areas, typically forests or bushes with thick and fertile soils (Zhao et al., 2018). In agricultural and natural environments, various fungi and bacteria are closely associated with plant (Gams et al., 2007; Tian et al., 2020), which positively regulate plant productivity and growth (Meesters et al., 2023). Microorganisms living in the soil (FAO 2003) provide various health benefits to the host plant (Srivastava et al., 2020). Evidence has shown that many beneficial soil-borne microorganisms have been found to boost the growth capacity of the aboveground parts of plants (Srivastava et al., 2020; Zhao et al., 2021). The reproductive growth stages of soybean plants are influenced by rhizosphere microbial communities (Xu et al., 2009). The roots of Arabidopsis colonized by the plant-control soil bacterium Bacillus subtilis FB17 greatly improves aboveground plant tissue growth (Berendsen et al., 2012). Bacillus spp. (Kim et al., 1997) and Trichoderma spp. (Duffy et al., 1996) can suppress the growth of Gaeumannomyces graminis var. tritici in wheat rhizosphere (Weller et al., 2015). Specific microorganisms directly or indirectly promote plant growth, which is efficacy influenced by the rest of the root or soil microbial community on plant health (Weller et al., 2019). Bacteria and fungi in the soil can impact and promote plant growth, increasing crop productivity. By taking advantage of the abundant forests in Lishui City, the development of a medicinal economy in the forests has improved land utilization. Interplanting P. cyrtonema Hua in Cunninghamia lanceolata forest to study rhizomes in different growing soil environments can further identify special beneficial microbes, which is important for conducting multi-omics studies on plant growth associated with microbes in the forest. To ensure that microbes and plant roots are more effective in the field, an understanding of the interactions between the soil microbiota communities is required. Moreover, few researches have systematically investigated the effects of soil microbiota on functional metabolites of P. cyrtonema in the wild and artificially cultivated fields in C. lanceolata forests. Therefore, it is necessary to study the different relationships between microorganisms in Polygonatum rhizomes cultivated in the wild and artificially planted soils without fertilizers in a C. lanceolata forest. Materials and methods Field treatments Wild and cultivated samples of P. cyrtonema were collected from plantations in Suichang Baima Mountain (28°37’28”N, 119°8’12”E; altitude 1,225.2 m), Zhejiang Province (Southeast, China), in April 2023. The P. cyrtonema rhizomes were grown for three years and randomly arranged in two C. lanceolata forests. In each habitat, wild and cultivated P. cyrtonema were selected randomly; all samples were more than 20 m apart at the time of collection to ensure the independence of each sample. Growth and biomass assay The wild and cultivated P. cyrtonema Hua rhizomes were age-controlled and of the same species and were both grown in a C. lanceolata forest for 3 years with temperatures ranging 15–24℃ and at an altitude of 1,225.2 m. Plant growth was assessed by measuring stem length (n = 12). Cultivated and wild rhizomes were washed twice with sterilized deionized water. Then, absorbent paper was used to absorb water and weigh the fresh rhizomes. Rhizome roots were removed, dried, and crushed into a powder. Polysaccharides in P. cyrtonema Hua powder was detected using the method described by Laulloo et al. (2003). P. cyrtonema soil sample collection The samples were collected on April 15, 2023. From each of these sites, we selected five P. cyrtonema Hua. We collected five soil cores (diameter = 4.0 cm, depth = 10 cm), and mixed them into a single composite soil sample after removing litter from the soil (Yang et al., 2021). The climate humidity was 95% and the mean temperature was 15–24℃. Approximately 5 g of fresh rhizosphere soil was collected, the soil was carried in dry ice and stored ultra-low temperature freezer (−80 °C) until these soil samples were used to test the fungi and bacteria abundance based on high throughput sequencing (Tian et al., 2021). We randomly collected five replicates of wild and cultivated root plants soils from C. lanceolata forests. Five soil samples from P. cyrtonema Hua were grown for three years in a wild field (wild), and another five soil samples from P. cyrtonema Hua were grown for three years in an artificial cultivation field (cultivated). The soil samples were used for microbial sequencing analysis. DNA extraction and amplification Soil DNA kit (Omega, USA) was used to extracted wild and artificially cultivated plant rhizome soil DNA, through the manufacturer’s protocol. The 1.0% agarose gel electrophoresis was used to determined the quality of the DNA, and a NanoDrop2000 spectrophotometer (Thermo Scientific, United States) was detected the concentration of the DNA. The ITS region of fungi (ITS1F/ITS2R) (Liu et al., 2016) and 16S rRNA gene of bacteria (338F/806R) (Huse et al., 2008) were amplified. According to the manufacturer’s instructions and quantified using Qubit 4.0 (Thermo Fisher Scientific, USA), the product of PCR was purified by the PCR Clean-Up Kit (Shanghai, China). The amplicon libraries were sequenced on an Illumina MiSeq PE300 platform by Majorbio Medical Technology Co., Ltd. (Shanghai, China) (Pang et al., 2022). Isolation and identification of fungi Isolation of potential fungi from the soil were incubated in potato dextrose agar (PDA) for 7 d at 28°C. ITS was amplified using the fungal primers ITS1F/ITS4R to isolate the strains (Liu et al., 2016). Nucleotide BLAST (https://blast.ncbi.nlm.nih.gov/) was aligned with the ITS (fungi) database to determine approximate phylogenetic affiliation. Statistical Analysis The microbiota of soil analysis was performed applying the Majorbio Cloud platform (https://cloud.majorbio.com). Data analysis was performed applying one-way analysis of variance followed by Tukey’s honest significant difference, and expressed as the mean ± SD. Statistical analyses the data was used by Prism 8 (GraphPad), and statistical significance was set at P < 0.05. The change in biomass of P. cyrtonema The cultivated P. cyrtonema plants displayed longer stems (108.6 ± 12.89 mm) than wild P. cyrtonema plants (63.4 ± 10.74 mm), suggesting that the cultivated soil microbial community may promote P. cyrtonema growth (Fig. 1A and C). Additionally, the size of the fresh rhizome was significantly heavier in the cultivated plants compared to the wild plants (Fig. S1). The cultivated P. cyrtonema plants displayed a three-year-old rhizome that was larger than that of the wild rhizome, compared with that of the wild plants (n = 5; average, 32.12 g; P < 0.05), the fresh weight of the cultivated plants was significantly heavier (n=5; average, 80.39g) (Fig. 1B and Fig. S1). The polysaccharide content of the cultivated plants was higher (25.61 ± 5.13 mg/g) compared with those in the wild plants (18.43 ± 1.74 mg/g) (Fig. 1D). This result suggests that artificial cultivated soil microorganisms had a positive effect on the biomass of P. cyrtonema Hua. Microbial community and diversity of P. cyrtonema soil Notably, the alpha diversity of both the fungal and bacterial communities was not significantly altered in the wild and cultivated soils (Shannon index and other alpha diversity indices, Tables S3 and S4). Principal component analysis (PCA) at the genus level revealed the fungal and bacterial community compositions were clear and well clustering in the soils from both the wild and cultivated samples via to the analysis of similarities (ANOSIM) test (Fig. 2A and B). The first principal coordinates of the conditions explained 29.89% (bacteria) and 19.64% (fungi) of the total variance (Fig. 2A and B). Wild and cultivated soils did not overlap, indicating that two soil compartments about the fungal communities were generally different. Analyses of community abundance also showed an increased abundance of the fungal genera Geminibasidium (10.22%), Basidiomycota (12.25%), Bifiguratus (7.09%), and Fusidium (1.90%) compared with cultivated soils (0.01%, 3.10%, 0%, and 0%, respectively). However, cultivated soil was an increased abundance of the fungal genera Saitozyma (14.06%), Archaeorhizomycetes (11.05%), and Metarhizium (2.6%) compared to wild soils (4.76%, 0.40%, and 1.30%, respectively). In addition, the bacterial genera Gemmataceae (5.05%) and Rokubacteriales (1.57%) were more abundant in the wild soils than in the cultivated soils (1.06% and 0.22%, respectively) (Fig. 2C and D). These results revealed that the microbiota Saitozyma and Archaeorhizomycetes in cultivated soils may had the impact on the development of P. cyrtonema plants. Potential and beneficial fungi and bacteria As a result of the detecting microbiome sequencing, concerning the differences in the microbiota between wild and cultivated rhizosphere soils, beneficial fungi were isolated from the soil of the plants. Additionally, some potentially biocontrol bacteria and fungi were isolated from the cultivated P. cyrtonema root soil (Fig. 3A). The proportions of Clonostachys divergens and Archaeorhizomycetes spp. were significantly higher in cultivated plant soil ( P < 0.05; Fig. 3B and D), but these fungi were significantly reduced in wild plants. Interestingly, some species of the fungal genus Clonostachys are used as a plant growth-promoting fungus in solanaceous fruit vegetables, tomatoes, peppers, and eggplants (Han et al., 2020). In addition, the proportions of Geminibasidium spp . and Bifiguratus spp . were clearly higher in the wild plant soil than in the cultivated plant soil. Wild soil microbiomes were associated with Geminibasidium and Bifiguratus fungi. Bifiguratus adelaidae may have a symbiotic function in the roots and has been detected in orchid and chestnut roots (Timothy et al., 2017). There are interesting similarities between B. adelaidae and Archaeorhizomyces (Rosling et al., 2011; 2013). Moreover, several bacteria of the genus Bacillus were significantly enriched in the cultivated soils ( P < 0.05; Fig. 3C). However, Geminibasidium and Rokubacteriales were detected in wild plant soil (Fig. 3A and C). Based on these results, the fungi Clonostachys divergens and Archaeorhizomycetes sp., and bacteria Bacillus were significantly enriched in the cultivated soil. Tracking changes in function To identify the beneficial fungi that affect the growth increased for P. cyrtonema , we isolated beneficial fungi and investigated their functions. The differences were evaluated by two-tailed Wilcoxon rank-sum test in the relative abundances of fungi and bacteria at the genus level between the wild and cultivated soils (Fig. 4A). Basidiomycota , Archaeorhizomycetes , Geminibasidium , Bifiguratus , and Rozellomycota were the significantly different fungal genera (Fig. 4A). A co-occurrence network was used to analyze the complexity of the connections within the rhizosphere soil microbiomes of P. cyrtonema . The cultivated plants showed a high level of complexity with negative and positive interactions, whereas the wild plants presented a less complex diversity of fungi (Fig. 4C). In addition, we isolated three fungi genera with the ITS sequence and performed BLAST in NCBI. Trichoderma spp ., Aspergillaceae spp . , and Mucor spp . (Fig 4B) as candidate biocontrol strains were identified to the Trichoderma , Aspergillaceae , and Mucor genera. The plate confrontation tests have shown their potential antifungal ability (Fig. 4B). In wild soil, the results showed that potentially pathogenic bacteria were largely enriched compared with cultivated plant soil (Fig. S2). In the FAPROTAX method, cultivated soil was more enriched by xylanolysis, aromatic compound degradation, nitrogen fixation and chemoheterotrophy, etc. The function heatmap showed that xylanolysis was remarkably upregulated in cultivated-type plants (Fig. S2). Discussion Recently, the important role of plant microbiota has been described. Beauveria , Metarhizium , Cladosporium , Clonostachys , and Isaria species can act as endophytes, providing many benefits to the plant, such as increased plant growth (Beneduzi et al., 2012; Bamisile et al., 2023). Although, the results of Alpha diversity analysis showed that the observed species number was lower in cultivated rhizosphere soil when compared with wild rhizosphere soil, which might be the result of artificial operation. In addition, the soil microbiota Clonostachys divergens and Archaeorhizomycetes spp. were significantly enriched in cultivated rhizosphere. Clonostachys rosea ST1140 is a plant growth-promoting fungus used in solanaceous fruit vegetables, tomatoes, peppers, and eggplants (Türkölmez et al., 2023). An increased abundance of the fungal genera Saitozyma (14.06%), Archaeorhizomycetes (11.05%) and Metarhizium (2.6%) in cultivated soil. Metarhizium brunneum promotes the growth of tomatoes following its endophytic establishment within plants after treatment with seeds, which primarily includes the enhancement of plant growth (Krell et al., 2018). M. robertsii endophytically colonizes tomato plants, resulting in their improved growth (Oliveira-Siqueira et al., 2020). The fungus Saitozyma spp. is more closely related to cultivated soils and is associated with coffee production (Veloso et al., 2023). Moreover, the proportion of sequences of Bacillus species was significantly enriched in cultivated rhizomes soils. Bacillus T8 and Bacillus OSU-142 (Arikan et al., 2016) have great potential to enhance the plant and wild growth of sour cherry; therefore, they have been recommended for promoting the sour cherry cultivation growth (Arikan et al., 2016). However, Geminibasidiales and Bifiguratus species were enriched in wild rhizomes soil of P. cyrtonema Hua. Geminibasidiales and Bifiguratus have unclear plant-associated functions. In addition, our results showed that the fresh weight and polysaccharide content of cultivated rhizomes were higher than those of wild rhizomes. The cultivated soil specifical microbes may play a key role for promoting the growth and activity of medicinal P. cyrtonema Hua, such as plant height, shoot length, and root weight. The co-occurrence of networks showed the dominance of positive correlations among potential interactions in the rhizosphere microbial community (Yu et al., 2022). The result showed that Mucoromycota positively interacted with Rozellomycota and negatively interacted with Ascomycota . Hyphal growth of Trichoderma sp. and Mucor sp. was inhibited by Aspergillus sp. Plant-beneficial fungi constitute a diverse group of fungi belonging to diverse genera (Meesters et al., 2023), such as Aspergillus , Penicillium , Fusarium, Trichoderma and Glomus (Hyakumachi et al., 1994; Singh et al., 2017), Entomopathogenic fungi, such as Metarhizium and Beauveria , have need to adopted an endophytic lifestyle that one of a diverse array of benefits were convenient for providing an nutrient for host plants (Gange et al., 2019; Vidal et al., 2015; Vega, 2018). In our result, the co-occurrence network showed a high level of complexity with negative and positive interactions in the cultivated rhizosphere soil. Some key microbes in the rhizosphere soil may have synergistic effects in increase growth of plant, and this potential cooperative relationship may be reinforced in the rhizosphere for broader biomass of P. cyrtonema Hua. In conclusion, our results have important implications for cultivating and managing the quality and productivity of P. cyrtonema Hua compared with wild plants. This may result in artificial management have an increase in one of the potentially medicinal active ingredients (e.g., polysaccharide content) of P. cyrtonema Hua. Beneficial microbes recruited to the plant rhizosphere and stably associated with C. lanceolata roots can potentially reduce biotic stress or increase the biomass according to management. Moreover, both wild and cultivated rhizosphere soil collected in C. lanceolata forests, C. lanceolata forest ecosystems may play an important role in the function of the interaction between rhizosphere microorganisms and P. cyrtonema Hua. In the future, research on microbial interactions involved in coping with pathogen attack are understood under C. lanceolata forest. Acknowledgments Financial support for this study was provided by grants from the Key Research and Development Program of Lishui City (2021ZDYF07) and the Doctoral Research Program of Lishui University (QDZK112023027). Conflict of interest statement All authors declared no conflicts of interest to this work. Data availability statement The data supporting the findings of this study are available from the corresponding author upon reasonable request. Figure legends Figure 1 . Rhizome growth analysis of wild and cultivated plants. A. The height of the plant stem in wild and cultivated plants; B. Fresh weight of two samples; C. Stem length of two samples; D. Polysaccharide content of two samples; t-test, P < 0.05. Figure 2 . Student’s t-test. (A and B) PCA of bacterial and fungal community beta diversity of two samples (ANOSIM; bacterial: R = 0.5880, P = 0.004; fungal: R = 0.4640, P = 0.004). (C and D) Relative abundance of the most abundant (≥ 15%) bacterial and fungal taxa in wild and cultivated plants. Figure 3. Relative abundance of species between wild and cultivated rhizomes; Wilcoxon rank sum test and t-test, P < 0.01. A. Relative abundance of Gemmataceae and Acidothermus ; B. Relative abundance of Clonostachys rdivergens and Bifiguratus spp.; C. Relative abundance of Bacillus and Rokubacteriales . Figure 4. A. Significance test between wild and cultivated rhizosphere soil fungal community groups, conducted via Wilcoxon rank sum test. B. Inhibitory effects of Aspergillus spp. on Trichoderma spp. and Mucor spp. C. Co-occurrence networks of initial microbiomes that later became associated with wild (left) and cultivated (right) plants. Figure S1 . Rhizome size. Figure S2. A. Function heatmap; B. Venn diagram of bacteria; C. Variations in phenotype composition in bacteria. Table S1. Sequence quality data in bacteria. Table S2. Sequence quality data in fungi. Table S3. 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Keywords bacteria fungi polygonatum cyrtonema hua soil microbiome Authors Affiliations Liu Haiyan View all articles by this author Sun Yingying View all articles by this author Hou Jing View all articles by this author zhou duan 0009-0000-3203-4182 [email protected] Lishui University View all articles by this author Metrics & Citations Metrics Article Usage 303 views 188 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Liu Haiyan, Sun Yingying, Hou Jing, et al. Diversity and function of rhizosphere microorganisms in medicinal plant Polygonatum cyrtonema Hua. Authorea . 09 March 2024. DOI: https://doi.org/10.22541/au.170995964.42772955/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . 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