Abstract
Few studies have examined the association of factors associated with soil fertility and composition with the structure of microbial communities in the rhizosphere and endosphere. Hence, this study aimed to explore the effects of geographical differences on fungal communities in the roots of Scrophularia ningpoensis and the relationship between the fungal communities and secondary metabolic components in the host plant. We found that there was greater diversity in the fungal communities of the rhizosphere compartment than in endosphere communities. Ascomycota and Basidiomycota were dominant among the endosphere fungi, whereas Mortierellomycota was distributed in the rhizosphere. The composition of bulk soil obtained from different producing areas was significantly different, and the correlation between the rhizospheric and physicochemical compartments of the soil was higher than that observed with the endophytic compartment. Redundancy analysis and canonical correspondence analysis of the rhizospheric and endophytic samples revealed that the organic matter, total organic carbon, total nitrogen, and Hg levels were adequately correlated with the composition of rhizospheric and endophytic fungal communities. Multiple linear regression analyses facilitated the identification of potentially beneficial fungi whose abundance was correlated with levels of secondary metabolites, such as harpagide and harpagoside. These fungi could potentially provide valuable information regarding the use of S. ningpoensis in the medicinal plant industry.
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References
Ren D, Shen Z, Qin L, Zhu B (2021) Pharmacology, phytochemistry, and traditional uses of Scrophularia ningpoensis Hemsl. J Ethnopharmacol 269:113688
Wei B, Jiang X, Zhang J, Shen D (2017) Research progress of pharmacological effects and cultivation process technology of Scrophularia ningpoensis Hemsl. J Anhui Agric Sci 45(28):2
Wang H, Wang Y, Kang C, Wang S, Zhang Y, Yang G, Zhou L, Xiang Z, Huang L, Liu D, Guo L (2022) Drought stress modifies the community structure of root-associated microbes that improve Atractylodes lancea growth and medicinal compound accumulation. Front Plant Sci 13:1032480
Han MF, Zhang LQ, Li YM (2017) Research progress on chemical structures and pharmacological effects of natural aucubin and its derivatives. Chin Tradit Herb Drug 48(19):4105–4113
Stassen MJJ, Hsu SH, Pieterse CMJ, Stringlis IA (2021) Coumarin coummunication along the microbio root-shoot axis. Trends Plant Sci 26(2):169–183
Jin T, Wang Y, Huang Y et al (2018) Erratum to: Taxonomic structure and functional association of foxtail millet root microbiome. GigaScience 7(11):1–12
Mitter EK, de Freitas JR, Germida JJ (2017) Bacterial root microbiome of plants growing in oil sands reclamation covers. Front Microbiol 8:849
Pascale A, Proietti S, Pantelides IS, Stringlis IA (2020) Modulation of the root microbiome by plant molecules: the basis for targeted disease suppression and plant growth promotion. Front Plant Sci 10:1741
Berg G, Smalla K (2010) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci USA 112(8):7911–7920
Shi J, Yuan X, Lin H, Yang Y, Li Z (2011) Differences in soil properties and bacterial communities between the rhizosphere and bulk soil and among different production areas of the medicinal plant Fritillaria thunbergii. Int J Mol Sci 12(6):3770–3785
Jia M, Chen L, Xin H, Zheng C, Rahman K, Han T, Qin LP (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906
Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247
Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124
Kusari S, Lamshöft M, Spiteller M (2009) Aspergillus fumigatus Fresenius, an endophytic fungus from Juniperus communis L. Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J Appl Microbiol 107:1019–1030
Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162
Kusari S, Verma VC, Lamshoeft M, Spiteller M (2012) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28:1287–1294
Zhu B, Wu J, Ji Q, Wu W, Dong S, Yu J, Zhang Q, Qin L (2020) Diversity of rhizosphere and endophytic fungi in Atractylodes macrocephala during continuous cropping. Peer J 8:e8905
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267
Siqueira GM, Dafonte JD, Valcárcel ArmestoFrança e Silva MÊF (2014) Using multivariate geostatistics to assess patterns of spatial dependence of apparent soil electrical conductivity and selected soil properties. Sci World J 2014:712403
Liu Z, Cai X, Liu T, Zhao C, Sun W, Zhu J (2022) Determination of total nitrogen content in soil with graphite digestion apparatus and Kjeldahl nitrogen determination method. Chem Anal Meterage 31(12):4
Peng G, Kang C, Zhong H, Hu Z, Hu G, Li J, Xia X (2011) Study on quality control index of total phosphorus in water by ammonium molybdate spectrophotometry. Environ Impact Asses 33(002):31–34
Yao Q, Liu J, Yu Z, Li Y, Jin J, Liu X, Wang G (2017) Three years of biochar amendment alters soil physiochemical properties and fungal community composition in a black soil of northeast China. Soil Biol Biochem 110:56–67
Ye C, Li S, Zhang Y, Zhang Q (2011) Assessing soil heavy metal pollution in the water-level-fluctuation zone of the Three Gorges Reservoir, China. J Hazard Mater 191(1–3):366–372
Yang Y, Li X, Tang O, Wang M, Li J, Zhu B, Qin L (2020) Diversity and community structure of endophytic fungi in Corydalis yanhusuo tuber and their correlations with tetrahydropalmatine content. Chin Her Med 51(7):8
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Met 7(5):335–336
González V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fung Diver 47:29–42
Hartman K, van der Heijden MG, Roussely-Provent V, Walser JC, Schlaeppi K (2017) Deciphering composition and function of the root microbiome of a legume plant. Microbiome 5(1):2
Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G, Podar M, Schadt CW (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature populus deltoides trees. PLoS ONE 8(10):e76382
Mesa V, Navazas A, González-Gil R, González A, Weyens N, Lauga B, Gallego JLR, Sánchez J, Peláez AI (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by autochthonous betula celtiberica. Appl Environ Microbiol 83(8):e03411-03416
Beckers B, Op De Beeck M, Weyens N, Boerjan W, Vangronsveld J (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5(1):25
Osińska-Jaroszuk M, Jarosz-Wilkołazka A, Jaroszuk-Ściseł J, Szałapata K, Nowak A, Jaszek M, Ozimek E, Majewska M (2015) Extracellular polysaccharides from Ascomycota and Basidiomycota: production conditions, biochemical characteristics, and biological properties. World J Microbiol Biotechnol 31(12):1823–1844
Wohlbach DJ, Thompson DA, Gasch AP, Regev A (2009) From elements to modules: regulatory evolution in Ascomycota fungi. Curr Opin Genet Dev 19(6):571–578
Yang C, Li J, Liu N, Zhang Y (2019) Effects of fairy ring fungi on plants and soil in the alpine and temperate grasslands of China. Plant Soil 441:499–510
Sepčić K, Sabotič J, Ohm RA, Drobne D, Jemec Kokalj A (2019) First evidence of cholinesterase-like activity in Basidiomycota. PLoS One 14(4):e0216077
Andrew DR, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG, Dontsova K (2012) Abiotic factors shape microbial diversity in sonoran desert soils. Appl Environ Microbiol 78(21):7527–7537
İnceoğlu Ö, Falcão Salles J, van Elsas JD (2012) Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb Ecol 63(2):460–470
Santos-González JC, Nallanchakravarthula S, Alström S, Finlay RD (2011) Soil, but not cultivar, shapes the structure of arbuscular mycorrhizal fungal assemblages associated with atrawberry. Microb Ecol 62(1):25–35
Acknowledgements
This study was supported by the Key Research and Development Program of Zhejiang Province of China (2021C04029), China; The Enshi Prefecture Science and technology program research and development project (D20210035), China; and Young Innovative Talents Project of Zhejiang Medical Health Science and Technology (2022RC052), China.
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Dan Ren performed the experiments, analyzed the data, and wrote and revised the manuscript; Kunyuan Guo and Qing-mei Sun performed the experiments, and prepared figures and tables. Bo Zhu and Lu-ping Qin conceived and designed the experiments, authored or reviewed drafts of the paper, and approved the final draft.
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Ren, D., Guo, K., Sun, Q. et al. Variations in Rhizospheric and Endophytic Root Fungal Communities of Scrophularia ningpoensis in Different Producing Areas. Curr Microbiol 80, 323 (2023). https://doi.org/10.1007/s00284-023-03439-1
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DOI: https://doi.org/10.1007/s00284-023-03439-1