Abstract
Purpose
This work integrated field investigation results with laboratory experiments to investigate the interaction of rhizosphere soil microorganisms in the continuous cropping of Panax notoginseng and saponins, providing a scientific foundation for overcoming P. notoginseng continuous cropping obstacles.
Methods
The concentrations of saponins were measured using UPLC–MS/MS, and the microbes in the P. notoginseng rhizosphere soil were sequenced using the Illumina MiSeq high-throughput platform.
Results
The concentrations of ginsenoside Rd, ginsenoside Rg2, ginsenoside Rg1, ginsenoside Re, ginsenoside Rb1 and notoginsenoside R1 in the rhizospheric soil of infected P. notoginseng increased considerably. The P. notoginseng rhizospheric soil rapidly degraded saponins in the following order: ginsenoside Rd > ginsenoside Rg1 > notoginsenoside R1 > ginsenoside Re > ginsenoside Rg2 > ginsenoside Rb1. Saponins substantially enhanced the fungal Chao1 index, and Rd had the greatest effect. Saponins shifted the microbial community architecture and abundance in the rhizosphere soil. Ginsenoside Re stimulated the growth of Rhodotorula and Alternaria, ginsenoside Rg1 significantly increased the production of Spizellomyces, ginsenoside Rd promoted the proliferation of Aureobasidium, and notoginsenoside R1 fostered the growth of Alternaria. Further investigations showed that increases in Plectosphaerella and Clonostachys were directly and positively related to notoginsenoside R1, ginsenoside Rg1, and ginsenoside Rb1, while an increase in Ilyonectria was strongly and positively related to ginsenoside Rb1 and ginsenoside Rg2.
Conclusions
The six saponins have the potential to shape the structure of the microbial community of the P. notoginseng rhizospheric soil, and enrichment in particular saponins lays the foundation for the emergence and proliferation of pathogenic fungi.
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Data availability
The datasets generated during the current study are available in the NCBI repository: https://www.ncbi.nlm.nih.gov/bioproject/PRJNA808393.
References
Baidu-Forson JJ, Hodgkin T, Jones M (2012) Introduction to special issue on agricultural biodiversity, ecosystems and environment linkages in Africa. Agr Ecosyst Environ 157:1–4. https://doi.org/10.1016/j.agee.2012.04.011
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Bao LM, Liu YY, Ding YF, Shang JJ, Wei YL, Tan Y, Zi FT (2022) Interactions Between Phenolic Acids and Microorganisms in Rhizospheric Soil From Continuous Cropping of Panax notoginseng. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.791603.
Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83. https://doi.org/10.1023/A:1026290508166
Bienapfl JC, Floyd CM, Percich JA, Malvick DK (2012) First Report of Clonostachys rosea Causing Root Rot of Soybean in the United States. Plant Dis 96:1700–1700. https://doi.org/10.1094/pdis-06-12-0550-pdn
Chuah TS, Tan PK, Ismail BS (2013) Effects of adjuvants and soil microbes on the phytotoxic activity of coumarin in combination with p-vanillin on goosegrass (Eleusine indica L.) seedling emergence and growth. S Afr J Bot 84:128–133. https://doi.org/10.1016/j.sajb.2012.11.003
Chinese Pharmacopoeia Commission (2015) Chinese Pharmacopoeia. Medical And Technology Press, Beijing. https://db.ouryao.com/yd2020/view.php?id=f2fd6c8074
Dong LL, Xu J, Feng GQ, Li XW, Chen SL (2016) Soil bacterial and fungal community dynamics in relation to Panax notoginseng death rate in a continuous cropping system. Sci Rep 6:31802. https://doi.org/10.1038/srep31802
Ehrmann J, Ritz K (2014) Plant: soil interactions in temperate multi-cropping production systems. Plant Soil 376:1–29. https://doi.org/10.1007/s11104-013-1921-8
Elsharkawy MM, Shimizu M, Takahashi H, Hyakumachi M (2012) Induction of systemic resistance against Cucumber mosaic virus by Penicillium simplicissimum GP17-2 in Arabidopsis and tobacco. Plant Pathol 61:964–976. https://doi.org/10.1111/j.1365-3059.2011.02573.x
Etalo DW, Jeon JS, Raaijmakers JM (2018) Modulation of plant chemistry by beneficial root microbiota. Nat Prod Rep 35:398–409. https://doi.org/10.1039/c7np00057j
Fu LN, Wang YT, Wang X, Ji GH, Wei LF (2018) The study on microbial diversity of rhizosphere in continuous cropping system of Panax notoginseng. J Yunnan Agric Univ 33:198–207. https://doi.org/10.12101/j.issn.1004-390X(n).20170303
Gao ZM, Li JH, Shen YC, Zhang HR, Zhang YX, Zhang ZL (2019) Effects of two kinds of saponins and Panax notoginseng saponins (PNS) on growth and physiology of Chinese cabbage seedlings. J Henan Agric Sci 48(94–98):104. https://doi.org/10.15933/j.cnki.1004-3268.2019.01.015
Gilardi G, Garibaldi A, Gullino ML (2013) Seed transmission of Plectosphaerella cucumerina, causal agent of leaf spot of Diplotaxis tenuifolia in Italy. Phytoparasitica 41:411–416. https://doi.org/10.1007/s12600-013-0302-4
Gong JT, Cheng XY, Sun M, Wu LJ, Zhang ZL (2015) Effects of three kinds of saponins on seed germination and seedling growth of Panax notoginseng. Acta Agric Univ Jiangxiensis 37:988–993. https://doi.org/10.13836/j.jjau.2015150
Guan YM, Ma YY, Jin Q, Wang QX, Liu N, Fu YP, Zhang YY, Li Y (2020) Multi-locus phylogeny and taxonomy of the fungal complex associated with rusty root rot of Panax ginseng in China. Front Microbiol 11:618942. https://doi.org/10.3389/fmicb.2020.618942
Guo LP, Huang LQ, Jiang YX, Chen ML, Lv DM, Zeng Y (2007) Change of microbial community in rhizoma sphere of cultivated Atractylodes lancea. China J Chin Materia Med 32:1131–1133. https://doi.org/10.3321/j.issn:1001-5302.2007.12.003
Hieno A, Naznin HA, Hyakumachi M, Higuchi-Takeuchi M, Matsui M, Yamamoto YY (2016) Possible involvement of MYB44-mediated stomatal regulation in systemic resistance induced by Penicillium simplicissimum GP17-2 in Arabidopsis. Microbes Environ 31:154–159. https://doi.org/10.1264/jsme2.ME16025
Huang XQ, Zhao J, Zhou X, Han YS, Zhang JB, Cai ZC (2019) How green alternatives to chemical pesticides are environmentally friendly and more efficient. Eur J Soil Sci 70:518–529. https://doi.org/10.1111/ejss.12755
Jae JW, Kyeong MP, An-Sik C (2011) Herbal medicine: biomolecular and clinical aspects, 2nd edn. CRC Press/Taylor & Francis, Boca Raton, FL https://ncbi.nlm.nih.gov/books/NBK92776/
Jia MY, Li QL, Hua J, Liu JY, Zhou W, Qu B, Luo SH (2020) Phytohormones regulate both "fish scale" galls and cones on Picea koraiensis. Front Plant Sci 11: 580155. https://doi.org/10.3389/fpls.2020.580155.
Jiao XL, Bi XB, Zhang XS, Gao WW (2015) Autotoxic effect of ginsenoside extrats on growth of American ginseng in different medium. China J Chin Materia Med 40:1433–1438. https://doi.org/10.4268/cjcmm20150802
Kautz T, Amelung W, Ewert F, Gaiser T, Horn R, Jahn R, Javaux M, Kemna A, Kuzyakov Y, Munch JC, Pätzold S, Peth S, Scherer HW, Schloter M, Schneider H, Vanderborght J, Vetterlein D, Walter A, Wiesenberg GLB, Köpke U (2013) Nutrient acquisition from arable subsoils in temperate climates: A review. Soil Biol Biochem 57:1003–1022. https://doi.org/10.1016/j.soilbio.2012.09.014
Kuczynski J, Stombaugh J, Walters WA, Gonzalez A, Caporaso JG, Knight R (2012) Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current protocols in microbiology Chapter 1: Unit 1E.5. https://doi.org/10.1002/9780471729259.mc01e05s27.
Leitao AL, Enguita FJ (2016) Gibberellins in Penicillium strains: challenges for endophyte-plant host interactions under salinity stress. Microbiol Res 183:8–18. https://doi.org/10.1016/j.micres.2015.11.004
Li QL, Xiao HL (2012) The interactions of soil properties and biochemical factors with plant allelopathy. Ecol Environ Sci 21:2031–2036. https://doi.org/10.16258/j.cnki.1674-5906.2012.12.013
Li YB, Liu JG, Cheng XR, Zhagn W, Sun YY (2009) The allelopathic effects of returning cotton stalk to soil on the growth of succeeding cotton. Acta Ecol Sin 29:4942–4948. https://doi.org/10.3321/j.issn:1000-0933.2009.09.042
Li Y, Ying YX, Zhao DY, Jin S, Ding WL (2010) Genetic diversity analysis on rhizosphere soil microbial population of Panax ginseng and Panax quinquefolium by RAPD. Chinese Traditional and Herbal Drugs 41:1871–1875
Li X-g, Ding C-f, Zhang T-l, Wang X-x (2014) Fungal pathogen accumulation at the expense of plant-beneficial fungi as a consequence of consecutive peanut monoculturing. Soil Biol Biochem 72:11–18. https://doi.org/10.1016/j.soilbio.2014.01.019
Li MJ, Feng FJ, Zhang B, Gu L, Wang FQ, Yang YH, Tian YH, Chen XJ, Zhang ZY (2017) Advances on molecular mechanisms of Rehmannia glutinosa consecutive monoculture problem formation in multi-omics era. China J Chin Materia Med 42:413–419. https://doi.org/10.19540/j.cnki.cjcmm.20170103.002
Li HC, Zuo YM, Yang SB, Yang TM, Li JC, Yang WZ, Zhang JY (2020a) Ecological effect of root exudates of Panax notoginseng on continuous Cropping obstacles and its alleviating methods. J Agric Sci Technol 22:159–167. https://doi.org/10.13304/j.nykjdb.2019.0594
Li YL, Dai SY, Wang BY, Jiang YT, Ma YY, Pan LL, Wu K, Huang XQ, Zhang J, Cai ZC, Zhao J (2020b) Autotoxic ginsenoside disrupts soil fungal microbiomes by stimulating potentially pathogenic microbes. Appl Environ Microbiol 86:e00130-e120. https://doi.org/10.1128/aem.00130-20
Lin GB, Wan DG, Wang RT, Yang XJ, Guo XH, Yan ZY (2010) Research on the effects of planting Salviae miltiorrhizae Bge. on soil microorganism flora characteristics. West China J Pharm Sci 25:438–443. https://doi.org/10.13375/j.cnki.wcjps.2010.04.002
Liu XC, Li XH (2021) Basic biostatistical tests and their R codes. Chin J Appl Entomol 58:220–232
Liu ZX, Zou K (2003) A survey on the study of Panax plants in Hubei province. Li Shizhen Medicine and Materia Medica Res 14:62–64
Liu JG, Li YB, Jiang GY, Bian XM, Li F, Geng W (2008) Effects of long-term continuous cropping of cotton and returning cotton stalk into field on soil biological activities. Allelopath J 21:299–305. https://doi.org/10.13287/j.1001-9332.2008.0177
Liu YJ, Liu WY, Chen L, Zhang HB, Wang GS (2010) Microbial community and its activities in canopy- and understory humus of two montane forest types in Ailao Mountains, Northwest China. J Appl Ecol 21:2257–2266. https://doi.org/10.13287/j.1001-9332.2010.0343
Liu X, Zhang JL, Gu TY, Zhang WM, Shen QR, Yin SX, Qiu HZ (2014) Microbial community diversities and taxa abundances in soils along a seven-year gradient of potato monoculture using high throughput pyrosequencing approach. Plos One 9:e86610. https://doi.org/10.1371/journal.pone.0086610
Louws FJ, Rivard CL, Kubota C (2010) Grafting fruiting vegetables to manage soilborne pathogens, foliar pathogens, arthropods and weeds. Sci Hortic 127:127–146. https://doi.org/10.1016/j.scienta.2010.09.023
Luo LF, Guo CW, Wang LT, Zhang JX, Deng LM, Luo KF, Huang HC, Liu YX, Mei XY, Zhu SS, Yang M (2019) Negative plant-soil feedback driven by re-assemblage of the rhizosphere microbiome with the growth of Panax notoginseng. Front Microbiol 10:1597. https://doi.org/10.3389/fmicb.2019.01597
Luo LF, Yang L, Yan ZX, Jiang BB, Li S, Huang HC, Liu YX, Zhu SS, Yang M (2020) Ginsenosides in root exudates of Panax notoginseng drive the change of soil microbiota through carbon source different utilization. Plant Soil 455:139–153. https://doi.org/10.1007/s11104-020-04663-5
Miao ZQ, Li SD, Liu XZ, Chen YJ, Li YH, Wang YT, Guo RJ, Xia ZY, Zhang KQ (2006) The causal microorganisms of Panax notoginseng root rot disease. Scientia Agricultura Sinica 39:1371–1378. https://doi.org/10.3321/j.issn:0578-1752.2006.07.011
Miao CP, Mi QL, Qiao XG, Zheng YK, Chen YW, Xu LH, Guan HL, Zhao LX (2016) Rhizospheric fungi of Panax notoginseng: diversity and antagonism to host phytopathogens. J Ginseng Res 40:127–134. https://doi.org/10.1016/j.jgr.2015.06.004
Nicol RW, Traquair JA, Bernards MA (2002) Ginsenosides as host resistance factors in American ginseng (Panax quinquefolius). Can J Bot-Revue Canadienne De Botanique 80:557–562. https://doi.org/10.1139/b02-034
Nicol RW, Yousef L, Traquair JA, Bernards MA (2003) Ginsenosides stimulate the growth of soilborne pathogens of American ginseng. Phytochemistry 64:257–264. https://doi.org/10.1016/s0031-9422(03)00271-1
Pei C (2016) Study on autotoxin-degrading bacteria in continuous cropping obstacle of Panax notoginseng. Zhejiang Sci-Tech University. https://kns.cnki.net/kcms2/article/abstract?v=ZOmZWXXfAiDnnM5M1I1HCS3SwzyIX0CcHC2bnj_N3O7zgd9KD1k6RYmZfbKQRuQy9qOj43KD6YvVIGVVROYAbaQdvmYH6sX6FPck67KQFjspyxiGS8XbA==&uniplatform=NZKPT&language=CHS
Qiao YJ, Gu CZ, Zhu HT, Wang D, Zhang MY, Zhang YX, Yang CR, Zhang YJ (2020) Allelochemicals of Panax notoginseng and their effects on various plants and rhizosphere microorganisms. Plant Diversity 42:323–333. https://doi.org/10.1016/j.pld.2020.04.003
Shen Y (2016) Allelopathic effects of phenolic acids and saponins on Panax notoginseng and three crop rotation seedlings. Henan Agricultural University, Zhengzhou. https://doi.org/10.7666/d.D01117070
Tan Y, Cui Y, Li H, Kuang A, Li X, Wei Y, Ji X (2017) Rhizospheric soil and root endogenous fungal diversity and composition in response to continuous Panax notoginseng cropping practices. Microbiol Res 194:10–19. https://doi.org/10.1016/j.micres.2016.09.009
Tsunoda T, van Dam NM (2017) Root chemical traits and their roles in belowground biotic interactions. Pedobiologia 65:58–67. https://doi.org/10.1016/j.pedobi.2017.05.007
Ulrike Baetz EM (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98. https://doi.org/10.1016/j.tplants.2013.11.006
Urbez-Torres JR, Peduto F, Gubler WD (2012) First report of Ilyonectria macrodidyma causing root rot of olive trees (Olea europaea) in California. Plant Dis 96:1378–1378. https://doi.org/10.1094/pdis-04-12-0330-pdn
Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10. https://doi.org/10.1016/j.soilbio.2007.07.002
Vives-Peris V, Molina L, Segura A, Gomez-Cadenas A, Maria PR (2018) Root exudates from citrus plants subjected to abiotic stress conditions have a positive effect on rhizobacteria. J Plant Physiol 228:208–217. https://doi.org/10.1016/j.jplph.2018.06.003
Wang LT, Yang DY, Deng LM, Li YW, Ma YY, Han GY, Huang HC, Zhu SS, Yang M (2020) Isolation and screening of antagonistic autotoxin-degrading bacteria inPanax notoginseng [(Burk.)F. H. Chen ] rhizosphere soil. J South Argic 51: 305-312. CNKI:SUN:GXNY.0.2020-02-009
Wei G, Dong L, Yang J, Zhang L, Xu J, Yang F, Cheng R, Xu R, Chen S (2018) Integrated metabolomic and transcriptomic analyses revealed the distribution of saponins in Panax notoginseng. Acta Pharmaceutica Sinica B 8:458–465. https://doi.org/10.1016/j.apsb.2017.12.010
Wu HM, Lin WX (2020) A commentary and development perspective on the consecutive monoculture problems of medicinal plants. Chin J Eco-Agric 28:775–793. https://doi.org/10.13930/j.cnki.cjea.190760
Wu ZX, Hao ZP, Zeng Y, Guo LP, Huang LQ, Chen BD (2015) Molecular characterization of microbial communities in the rhizosphere soils and roots of diseased and healthy Panax notoginseng. Antonie Van Leeuwenhoek 108:1059–1074. https://doi.org/10.1007/s10482-015-0560-x
Wu HM, Wu LK, Wang JY, Zhu Q, Lin S, Xu JH, Zheng CL, Chen J, Qin XJ, Fang CX, Zhang ZX, Azeem S, Lin WX (2016a) Mixed phenolic acids mediated proliferation of pathogens Talaromyces helicus and Kosakonia sacchari in continuously monocultured Radix pseudostellariae rhizosphere soil. Front Microbiol 7:335. https://doi.org/10.3389/fmicb.2016.00335
Wu HM, Wu LK, Wang JY, Zhu Q, Xu JH, Zheng CL, Lin WX (2016b) The mechanisms of the rhizosphere management on the remission in consecutive monoculture problem and the improvement of soil quality. Ecologic Sci 35:225–232. https://doi.org/10.14108/j.cnki.1008-8873.2016.05.03
Xiang W (2016) Autotoxicity in Panax notoginseng of root exudates and their allelochemicals. Guangxi University, Guangxi. https://doi.org/10.7666/d.Y3086834
Xiao CP, Yang LM, Zhang LX, Liu CJ, Han M (2016) Effects of cultivation ages and modes on microbial diversity in the rhizosphere soil of Panax ginseng. J Ginseng Res 40:28–37. https://doi.org/10.1016/j.jgr.2015.04.004
Xiong W, Li R, Ren Y, Liu CJ, Zhao QY, Wu HS, Jousset A, Shen QR (2017) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207. https://doi.org/10.1016/j.soilbio.2017.01.010
Xu LH, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M (2012) Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biol Biochem 46:26–32. https://doi.org/10.1016/j.soilbio.2011.11.010
Yang M, Mei XY, Zheng JF, Yin ZB, Zhao Z, Zhang XD, He XH, Zhu SS (2014) Sensitivity of the pathogens of Panax notoginseng to ginsenosides. Plant Prot 40:76–81
Yang M, Zhang XD, Xu YG, Mei XY, Jiang BB, Liao JJ, Yin ZB, Zheng JF, Zhao Z, Fan LM, He XH, Zhu YQ, Zhu SS (2015) Autotoxic Ginsenosides in the Rhizosphere Contribute to the Replant Failure of Panax notoginseng. PloS one 10:e0118555. https://doi.org/10.1371/journal.pone.0118555
Yang JZ, Guan HL, Liu DH, Sun YQ, Wei ML, Wang YT (2016) Study on mechanism of Sanqi(Panax notoginseng F.H.Chen) replant failure and its alleviation technology. Northern Horticult: 160–163. https://doi.org/10.11937/bfyy.201614040.
Zhang AH, Lei FJ, Xu YH, Zhou GX, Zhang LX (2009) Effects of ginsenosides on the germinating of ginseng seeds and on the activity of antioxidant enzymes of the radicles of ginseng seedlings in vitro. Acta Ecol Sin 29:4934–4941. https://doi.org/10.3321/j.issn:1000-0933.2009.09.041
Zhang AH, Lei FJ, Fu JF, Zhou R, Zhang LX (2017a) Influence of exogenous ginsenosides on new forest soil microbial communities. China J Chin Materia Med 42:4756–4761. https://doi.org/10.19540/j.cnki.cjcmm.2017.0213
Zhang JY, Sun XT, Long GQ, Zhang GH, Meng GZ, Li LG, Yang SC, Chen JW (2017b) Influence of residual roots on growth of Panax notoginseng. Guangdong Agric Sci 044:27–38. https://doi.org/10.16768/j.issn.1004-874X.2017.06.005
Zhang HY, Xue QH (2010) Research progress in control of continuous cropping obstacle in Ginseng. Acta Agriculturae Jiangxi 022:68–71. https://doi.org/10.19386/j.cnki.jxnyxb.2010.06.022.
Zhao JM, Cui XM, Zeng HC, Yang JZ, Ma N, Zhang WB, Zhu L (2009) Study on chemical composition of root exudates from Panax notoginseng. Special Wild Econ Anim Plant Res 31:37–39. https://doi.org/10.16720/j.cnki.tcyj.2009.03.006
Zhao J, Li YL, Wang BY, Huang XQ, Yang L, Lan T, Zhang JB, Cai ZC (2017a) Comparative soil microbial communities and activities in adjacent Sanqi ginseng monoculture and maize-Sanqi ginseng systems. Appl Soil Ecol 120:89–96. https://doi.org/10.1016/j.apsoil.2017.08.002
Zhao J, Mei Z, Zhang X, Xue C, Zhang CZ, Ma TF, Zhang SS (2017b) Suppression of Fusarium wilt of cucumber by ammonia gas fumigation via reduction of Fusarium population in the field. Sci Rep 7:43103. https://doi.org/10.1038/srep43103
Zhou YC, Diao FQ, Liang N, Qu Y, Lu XY, Zhang FW (2003) Determination of the contents of ginsenoside Rg1, Re, Rb1 and the notoginsenoside R1 in the total notoginsenosides of the Panax notogineseng (Burk.)F.H.Chen by HPLC. J Shenyang Pharm Univ 20:27–31. https://doi.org/10.14066/j.cnki.cn21-1349/r.2003.01.009
Zhu LX, Zhang JE, Liu WG (2003) Review of studies on interactions between root exudates and rhizopheric microorganisms. Ecol Environ 12:102–105. https://doi.org/10.16258/j.cnki.1674-5906.2003.01.025
Acknowledgements
We are grateful to Guangzhou Gene Denovo Biotechnology Co., Ltd., for assisting with sequencing and bioinformatics analysis.
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This work was financially supported by the National Natural Science Foundation of China (Grant nos. 31960630 and 31960232).
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All authors contributed to the study conception and design. Materials preparation, data collection and analysis were performed by Limei Bao, Yuyan Liu, Jinmiao Chen, Yafang Ding, Junjie Shang, Jinhua Li, Yunlin Wei, Yong Tan and Futing Zi. The first draft of the manuscript was written by Limei Bao, and all the authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.
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Bao, L., Liu, Y., Chen, J. et al. Different effects of six saponins on the rhizosphere soil microorganisms of Panax notoginseng. Plant Soil 487, 389–406 (2023). https://doi.org/10.1007/s11104-023-05934-7
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DOI: https://doi.org/10.1007/s11104-023-05934-7