Elucidating the interaction of rhizosphere microorganisms and environmental factors influencing the quality of Polygonatum kingianum Coll. et Hemsl.
Polygonatum kingianum
Herb quality
Microbial diversity
Rhizosphere microorganism
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
17 Aug 2024
17 Aug 2024
Historique:
received:
21
06
2024
accepted:
07
08
2024
medline:
18
8
2024
pubmed:
18
8
2024
entrez:
17
8
2024
Statut:
epublish
Résumé
Polygonatum kingianum Collett & Hemsl., is one of the most important traditional Chinese medicines in China. The purpose of this study is to investigate the relationship between herb quality and microbial-soil variables, while also examining the composition and structure of the rhizosphere microbial community in Polygonatum kingianum, the ultimate goal is to provide a scientific approach to enhancing the quality of P. kingianum. Illumina NovaSeq technology unlocks comprehensive genetic variation and biological functionality through high-throughput sequencing. And in this study it was used to analyze the rhizosphere microbial communities in the soils of five P. kingianum planting areas. Conventional techniques were used to measure the organic elements, pH, and organic matter content. The active ingredient content of P. kingianum was identified by High Performance Liquid Chromatography (HPLC) and Colorimetry. A total of 12,715 bacterial and 5487 fungal Operational Taxonomic Units (OTU) were obtained and taxonomically categorized into 81 and 7 different phyla. Proteobacteria, Bacteroidetes, and Acidobacteriae were the dominant bacterial phyla Ascomycota and Basidiomycota were the dominat fungal phyla. The key predictors for bacterial community structure included hydrolysable nitrogen and available potassium, while for altering fungal community structure, soil organic carbon content (OCC), total nitrogen content (TNC), and total potassium content (TPOC) were the main influencing factors. Bryobacter and Candidatus Solibacter may indirectly increase the polysaccharide content of P. kingianum, and can be developed as potential Plant Growth Promoting Rhizobacteria (PGPR). This study has confirmed the differences in the soil and microorganisms of different origins of P. kingianum, and their close association with its active ingredients. And it also broadens the idea of studying the link between plants and microorganisms.
Identifiants
pubmed: 39154075
doi: 10.1038/s41598-024-69673-0
pii: 10.1038/s41598-024-69673-0
doi:
Substances chimiques
Nitrogen
N762921K75
Soil
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
19092Informations de copyright
© 2024. The Author(s).
Références
Xu, Y. L., Wang, Y. Z., Yang, M. Q. & Zhang, J. Y. Textual research on Polygonati rhizoma and ethnic usage. Chin. J. Exp. Trad. Med. Formulae 27, 237–250 (2021).
Li, X. C. et al. Steroid saponins from Polygonatum kingianum. Phytochemistry 31, 3559–3563 (1992).
pubmed: 1368862
doi: 10.1016/0031-9422(92)83727-G
Wang, Y. F., Lu, C. H., Lai, G. F., Cao, J. X. & Luo, S. D. A new indolizinone from Polygonatum kingianum. Planta Med. 69, 1066–1068 (2003).
pubmed: 14735451
doi: 10.1055/s-2003-45160
Baudoin, E., Benizri, E. & Guckert, A. Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol. Biochem. 35, 1183–1192 (2003).
doi: 10.1016/S0038-0717(03)00179-2
Vessey, J. K. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571–586 (2003).
doi: 10.1023/A:1026037216893
Mendes, L. W., Kuramae, E. E., Navarrete, A. A., Veen, J. A. & Tsai, S. M. Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J. 8, 1577–1587 (2014).
pubmed: 24553468
pmcid: 4817605
doi: 10.1038/ismej.2014.17
Shang, J. & Liu, B. Application of a microbial consortium improves the growth of Camellia sinensis and influences the indigenous rhizosphere bacterial communities. J. Appl. Microbiol. 130, 2029 (2020).
pubmed: 33170985
doi: 10.1111/jam.14927
Wang, L., Li, Z. Y., Liu, R. R., Li, L. L. & Wang, W. W. Bacterial diversity in soybean rhizosphere soil at seedling and mature stages. Pol. J. Microbiol. 68, 281–284 (2019).
pubmed: 31250597
pmcid: 7256853
doi: 10.33073/pjm-2019-023
Zi, H. Y., Jiang, Y. L., Cheng, X. M., Li, W. T. & Huang, X. X. Change of rhizospheric bacterial community of the ancient wild tea along elevational gradients in Ailao mountain, China. Sci. Rep. 10, 9203 (2020).
pubmed: 32514187
pmcid: 7280300
doi: 10.1038/s41598-020-66173-9
Bais, H. P., Prithiviraj, B., Jha, A. K., Ausubel, F. M. & Vivanco, J. M. Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434, 217–221 (2005).
pubmed: 15759001
doi: 10.1038/nature03356
Peiffer, J. A. et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. 110, 6548–6553 (2013).
pubmed: 23576752
pmcid: 3631645
doi: 10.1073/pnas.1302837110
Qin, D. et al. Microbial assemblages of Schisandraceae plants and the correlations between endophytic species and the accumulation of secondary metabolites. Plant Soil 483, 85–107 (2023).
doi: 10.1007/s11104-022-05729-2
Tang, S. et al. Impact of N application rate on tea (Camellia sinensis) growth and soil bacterial and fungi communities. Plant Soil 475, 343–359 (2022).
doi: 10.1007/s11104-022-05372-x
Fradin, E. F. & Thomma, B. P. H. J. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 7, 71–86 (2006).
pubmed: 20507429
doi: 10.1111/j.1364-3703.2006.00323.x
Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).
pubmed: 17586664
pmcid: 1950982
doi: 10.1128/AEM.00062-07
Magoc, T. & Salzberg, S. L. FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).
pubmed: 21903629
pmcid: 3198573
doi: 10.1093/bioinformatics/btr507
Wang, Y. F., Liu, L., Yue, F. X. & Li, D. Dynamics of carbon and nitrogen storage in two typical plantation ecosystems of different stand ages on the Loess Plateau of China. PeerJ 7, e7708 (2019).
pubmed: 31579599
pmcid: 6754723
doi: 10.7717/peerj.7708
Li, Y. et al. Humic acid fertilizer improved soil properties and soil microbial diversity of continuous cropping peanut: A three-year experiment. Sci. Rep. 9, 12014 (2019).
pubmed: 31427666
pmcid: 6700118
doi: 10.1038/s41598-019-48620-4
Gregory, J. C. et.al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 7, 335–336 (2010).
doi: 10.1038/nmeth.f.303
Adrain, J. M., Westrop, S. R., Chatterton, B. D. E. & Ramsköld, L. Silurian trilobite alpha diversity and the end-Ordovician mass extinction. Paleobiology 26, 625–646 (2000).
doi: 10.1666/0094-8373(2000)026<0625:STADAT>2.0.CO;2
Chao, A. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11(4), 265–270 (1984).
Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C. & Moënne-Loccoz, Y. The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321, 341–361 (2009).
doi: 10.1007/s11104-008-9568-6
Zhou, L. S., Li, H., Zhang, Y., Han, S. Q. & Xu, H. Development of genus-specific primers for better understanding the diversity and population structure of Sphingomonas in soils. J. Basic Microbiol. 54, 880–888 (2014).
pubmed: 23686867
doi: 10.1002/jobm.201200679
Hu, L. F. et al. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat. Commun. 9, 2738 (2018).
pubmed: 30013066
pmcid: 6048113
doi: 10.1038/s41467-018-05122-7
Tan, S. Y. et al. The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl. Soil Ecol. 64, 15–22 (2013).
doi: 10.1016/j.apsoil.2012.10.011
Berg, G. et al. Plant microbial diversity is suggested as the key to future biocontrol and health trends. FEMS Microbiol. Ecol. 93, 1–9 (2017).
doi: 10.1093/femsec/fix050
Ling, N. et al. The response of root-associated bacterial community to the grafting of watermelon. Plant Soil 391, 253–264 (2015).
doi: 10.1007/s11104-015-2399-3
Berlanas, C. et al. The fungal and bacterial rhizosphere microbiome associated with grapevine rootstock genotypes in mature and young vineyards. Front. Microbiol. 10, 1142 (2019).
pubmed: 31178845
pmcid: 6538693
doi: 10.3389/fmicb.2019.01142
Bulgarelli, D. et al. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17, 392–403 (2015).
pubmed: 25732064
pmcid: 4362959
doi: 10.1016/j.chom.2015.01.011
Zuo, J. J., Zu, M. T., Liu, L., Song, X. M. & Yuan, Y. D. Composition and diversity of bacterial communities in the rhizosphere of the Chinese medicinal herb Dendrobium. BMC Plant Biol. 21, 127 (2021).
pubmed: 33663379
pmcid: 7931511
doi: 10.1186/s12870-021-02893-y
Xu, J. et al. The structure and function of the global citrus rhizosphere microbiome. Nat. Commun. 9, 4894 (2018).
pubmed: 30459421
pmcid: 6244077
doi: 10.1038/s41467-018-07343-2
Zhao, J. et al. Influence of straw incorporation with and without straw decomposer on soil bacterial community structure and function in a rice-wheat cropping system. Appl. Microbiol. Biotechnol. 101, 4761–4773 (2017).
pubmed: 28197689
doi: 10.1007/s00253-017-8170-3
Upchurch, R. A. et al. Differences in the composition and diversity of bacterial communities from agricultural and forest soils. Soil Biol. Biochem. 40, 1294–1305 (2008).
doi: 10.1016/j.soilbio.2007.06.027
Priyadharsini, P. & Dhanasekaran, D. Diversity of soil Allelopathic Actinobacteria in Tiruchirappalli district, Tamilnadu, India. J. Saudi Soc. Agric. Sci. 14, 54–60 (2015).
Cho, H., Kim, M., Tripathi, B. M. & Adams, J. M. Changes in soil fungal community structure with increasing disturbance frequency. Microbial Ecol. 74, 62–77 (2016).
doi: 10.1007/s00248-016-0919-1
Lazzaro, A., Hilfiker, D. & Zeyer, J. Structures of microbial communities in Alpine soils: Seasonal and elevational effects. Front. Microbiol. 6, 1330 (2015).
pubmed: 26635785
pmcid: 4660872
doi: 10.3389/fmicb.2015.01330
Naether, A. et al. Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl. Environ. Microbiol. 78, 7398–7406 (2012).
pubmed: 22885760
pmcid: 3457104
doi: 10.1128/AEM.01325-12
Ramirez, K. S., Craine, J. M. & Fierer, N. Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob. Change Biol. 18, 1918–1927 (2012).
doi: 10.1111/j.1365-2486.2012.02639.x
Brewer, T. E., Handley, K. M., Carini, P., Gilbert, J. A. & Fierer, N. Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’. Nat. Microbiol. 2, 16198 (2017).
doi: 10.1038/nmicrobiol.2016.198
Zhou, X. G. & Wu, F. Z. p-Coumaric acid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f. sp. cucumerinum owen. PLoS ONE 7, e48288 (2012).
pubmed: 23118972
pmcid: 3484048
doi: 10.1371/journal.pone.0048288
Dong, Y., Dong, K., Zheng, Y., Tang, L. & Yang, Z. Faba bean fusarium wilt (Fusarium oxysporum) control and its mechanism in different wheat varieties and faba bean intercropping system. J. Appl. Ecol. 25, 1979–1987 (2014).
Gaspar, Y. M. et al. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J. Exp. Bot. 65, 1541–1550 (2014).
pubmed: 24502957
pmcid: 3967090
doi: 10.1093/jxb/eru021
Kara, E. L., Hanson, P. C., Hu, Y. H., Winslow, L. A. & McMahon, K. D. A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA. ISME J. 7, 680–684 (2013).
pubmed: 23051691
doi: 10.1038/ismej.2012.118
Zhang, B. G., Zhang, J., Liu, Y., Shi, P. & Wei, G. H. Co-occurrence patterns of soybean rhizosphere microbiome at a continental scale. Soil Biol. Biochem. 118, 178–186 (2018).
doi: 10.1016/j.soilbio.2017.12.011
Faust, K. & Raes, J. Microbial interactions: From networks to models. Nat. Rev. Microbiol. 10, 538–550 (2012).
pubmed: 22796884
doi: 10.1038/nrmicro2832
Zhao, Z. et al. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome 7, 33 (2019).
pubmed: 30813951
pmcid: 6393985
doi: 10.1186/s40168-019-0647-0
Fan, K. K. et al. Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment. ISME J. 15, 550–561 (2020).
pubmed: 33028975
pmcid: 8027226
doi: 10.1038/s41396-020-00796-8
Lu, L. H. et al. Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biol. Biochem. 65, 186–194 (2013).
doi: 10.1016/j.soilbio.2013.05.025
Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: Networks, competition, and stability. Science 350, 663–666 (2015).
pubmed: 26542567
doi: 10.1126/science.aad2602
Lear, G., Bellamy, J., Case, B. S., Lee, J. E. & Buckley, H. L. Fine-scale spatial patterns in bacterial community composition and function within freshwater ponds. ISME J. 8(8), 1715–1726 (2014).
pubmed: 24577354
pmcid: 4817609
doi: 10.1038/ismej.2014.21
Ranjard, L. et al. Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity. Nat. Commun. 4, 1434 (2013).
pubmed: 23385579
doi: 10.1038/ncomms2431
Ma, B. et al. Distinct biogeographic patterns for Archaea, Bacteria, and Fungi along the vegetation gradient at the continental scale in Eastern China. mSystems 2, e00174 (2017).
pubmed: 28191504
pmcid: 5296412
doi: 10.1128/mSystems.00174-16
Fukami, T. Historical contingency in community assembly: Integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).
doi: 10.1146/annurev-ecolsys-110411-160340
Moeller, A. H. et al. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc. Natl. Acad. Sci. 114, 13768–13773 (2017).
pubmed: 29229828
pmcid: 5748161
doi: 10.1073/pnas.1700122114
Qi, X. J., Wang, E. S., Xing, M., Zhao, W. & Chen, X. Rhizosphere and non-rhizosphere bacterial community composition of the wild medicinal plant Rumex patientia. World J. Microbiol. Biotechnol. 28, 2257–2265 (2012).
pubmed: 22806049
doi: 10.1007/s11274-012-1033-2
Khalediyan, N., Weisany, W. & Schenk, P. M. Arbuscular mycorrhizae and rhizobacteria improve growth, nutritional status and essential oil production in Ocimum basilicum and Satureja hortensis. Ind. Crops Prod. 160, 113–163 (2020).
Vafadar, F., Amooaghaie, R. & Otroshy, M. Effects of plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungus on plant growth, stevioside, NPK, and chlorophyll content of Stevia rebaudiana. J. Plant Interact. 9, 128–136 (2014).
doi: 10.1080/17429145.2013.779035
Bharti, N., Yadav, D., Barnawal, D., Maji, D. & Kalra, A. Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J. Microbial. Biotechnol. 29, 379–387 (2013).
doi: 10.1007/s11274-012-1192-1
Shuai, S. et al. Studies on the composition and diversity of seagrass Ruppia sinensis rhizosphere mmicroorganisms in the Yellow River Delta. Plants 12, 1435 (2023).
doi: 10.3390/plants12071435
Nagarajan, S. et al. Chapter 15—Actinobacterial enzymes—An approach for engineering the rhizosphere microorganisms as plant growth promotors. In Rhizosphere Engineering (eds Nagarajan, S. et al.) 273–292 (Elsevier, 2022).
Shi, Z. B., Yang, Y. M., Fan, Y. H., He, Y. & Li, T. Dynamic responses of rhizosphere microorganisms to biogas slurry combined with chemical fertilizer application during the whole life cycle of rice growth. Microorganisms 7, 1755 (2023).
doi: 10.3390/microorganisms11071755
Meng, L. B., Cheng, Z. Y. & Li, S. M. Response of soil nitrogen-cycling genes to the coupling effects of arbuscular mycorrhizal fungi inoculation and biochar application in maize rhizosphere. Sustainability 8, 1 (2024).
Wang, C. et al. Effects of hot pepper stalks on rhizosphere microflora structure of Polygonatum kingianum. Microbiol. China 1, 1–21 (2022).
Beeckmans, S. & Xie, J. P. Glyoxylate cycle. In Reference Module in Biomedical Sciences (eds Beeckmans, S. & Xie, J. P.) (Elsevier, 2015).
Yuan, M. M. et al. Climate warming enhances microbial network complexity and stability. Nat. Clim. Change 11, 343–348 (2021).
doi: 10.1038/s41558-021-00989-9
Wang, C. Y., Pei, X. H., Yue, S. S. & Wen, Y. N. The response of Spartina alterniflora biomass to soil factors in Yancheng, Jiangsu Province, P.R. China. Wetlands 36, 229–235 (2016).
doi: 10.1007/s13157-016-0732-0
Xiao, X., Fan, M. C., Wang, E. T., Chen, W. M. & Wei, G. H. Interactions of plant growth-promoting rhizobacteria and soil factors in two leguminous plants. Appl. Microbiol. Biotechnol. 101, 8485–8497 (2017).
pubmed: 29038972
doi: 10.1007/s00253-017-8550-8