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Root rot-infected Sanqi ginseng rhizosphere harbors dynamically pathogenic microbiotas driven by the shift of phenolic acids

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Abstract

Background and aims

Root rot is a catastrophic disease of perennial medicinal plants which could be caused by various soil-borne fungal pathogens. However, the understanding of the composition and diversity of root rot pathogenic fungi, their successions and potential drivers remains limited.

Methods

Sanqi ginseng (Panax notoginseng) was selected as a model plant and the rhizosphere soils of root rot-infected Sanqi ginseng at different growth years were collected. Phenolic acid content, pathogen abundance, and fungal microbiota were examined by using the high-performance liquid chromatography (HPLC), real-time PCR and Miseq sequencing.

Results

Pathogenic agents dominated in the rhizospheric fungal microbiota of rotten Sanqi ginseng and mainly comprised of Ilyonectria, Plectosphaerella, Clonostachys, Gibberella, Pestalotiopsis, Fusarium, and Chalara, with Ilyonectria and Fusarium being most abundant. The composition of pathogenic microbiota, but not α-diversity indices, changed considerably with Sanqi ginseng growth. The shifts of phenolic acid profile were an important driver in changes of rhizosphere pathogenic microbiota, and same phenolic acid exerted distinct functions on differential pathogenic taxa. Particularly, the contents of p-coumaric acid, ferulic acid, and benzoic acid were positively correlated with the abundance of genus Fusarium and negatively correlated with the abundance of genus Ilyonectria.

Conclusions

Root rot-infected Sanqi ginseng rhizosphere harbors dynamically pathogenic microbiota driven by the shift of phenolic acids. This study provides insights into the composition, variation, and driver of root rot pathogenic microbiota; these insights are important for the development of targeted measure for the prevention and control of root rot diseases.

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References

  • Aiello D, Guarnaccia V, Vitale A, Cirvilleri G, Granata G, Epifani F, Perrone G, Polizzi G, Groenewald JZ, Crous PW (2014) Ilyonectria palmarum sp. nov. causing dry basal stem rot of Arecaceae. Eur J Plant Pathol 138:347–359

    Article  CAS  Google Scholar 

  • Aoki T, O’Donnell K, Geiser DM (2014) Systematics of key phytopathogenic Fusarium species: current status and future challenges. J Gen Plant Pathol 80:189–201

    Article  CAS  Google Scholar 

  • Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai F, Chen W, Wei Z, Pang G, Li R, Ran W, Shen QR (2015) Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant Soil 388:337–350

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One 8:e55731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Yu H, Zhou X, Wu F (2018) Cucumber (Cucumis sativus L.) seedling rhizosphere Trichoderma and Fusarium spp. communities altered by vanillic acid. Front Microbiol 9:2195

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Liu Z, Qiu W, Tan X, Li J (2014) The main diseases and control measures of Panax notoginseng (Burk) F. H. Chen in Wuzhou City. Plant Di Pests 5:35–37

    Google Scholar 

  • Dong L, Xu J, Feng G, Li X, Chen S (2016) Soil bacterial and fungal community dynamics in relation to Panax notoginseng death rate in a continuous cropping system. Sci Rep 6:31802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong L, Xu J, Zhang L, Cheng R, Wei G, Su H, Yang J, Qian J, Xu R, Chen S (2018) Rhizospheric microbial communities are driven by Panax ginseng at different growth stages and biocontrol bacteria alleviates replanting mortality. Acta Pharm Sin B 8:272–282

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farh ME-A, Kim Y-J, Kim Y-J, Yang D-C (2018) Cylindrocarpon destructans/Ilyonectria radicicola-species complex: causative agent of ginseng root-rot disease and rusty symptoms. J Gin Res 42:9–15

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Guo HB, Cui XM, An N, Cai GP (2010) Sanchi ginseng (Panax notoginseng (Burkill) FH Chen) in China: distribution, cultivation and variations. Genet Resour Crop Ev 57:453–460

    Article  Google Scholar 

  • Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Hartmann A, Schmid M, Dv T, Berg G (2008) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Huang X, Zhou X, Zhang J, Cai Z (2019) Highly connected taxa located in the microbial network are prevalent in the rhizosphere soil of healthy plant. Biol Fert Soils 55:299–312

    Article  Google Scholar 

  • Hugoni M, Luis P, Guyonnet J, Haichar FZ (2018) Plant host habitat and root exudates shape fungal diversity. Mycorrhiza 28:451–463

    Article  PubMed  Google Scholar 

  • Jiang J, Yu M, Hou R, Li L, Ren X, Jiao C, Yang L, Xu H (2019) Changes in the soil microbial community are associated with the occurrence of Panax quinquefolius L. root rot diseases. Plant Soil 438:143–156

    Article  CAS  Google Scholar 

  • Jiang N, Qin LY, Ye YF (2011) Research advances in diseases of Panax notoginseng. J Sou Agr 42:1070–1074

    Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  CAS  Google Scholar 

  • Li X, Ding C, Zhang T, Wang 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

    Article  CAS  Google Scholar 

  • Li Y, Dai S, Wang B, Jiang Y, Ma Y, Pan L, Wu K, Huang X, Zhang J, Cai Z, Zhao J (2020) Autotoxic ginsenoside disrupts soil fungal microbiomes by stimulating potentially pathogenic microbes. Appl Environ Microbiol 86:e00130–e00120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lievens B, Brouwer M, Vanachter ACRC, Lévesque CA, Cammue B, Thomma BPHJ (2005) Quantitative assessment of phytopathogenic fungi in various substrates using a DNA macroarray. Environ Microbiol 7:1698–1710

    Article  CAS  PubMed  Google Scholar 

  • Ling N, Raza W, Ma JH, Huang QW, Shen QR (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47:374–379

    Article  CAS  Google Scholar 

  • Liu J, Li X, Jia Z, Zhang T, Wang X (2017) Effect of benzoic acid on soil microbial communities associated with soilborne peanut diseases. Appl Soil Ecol 110:34–42

    Article  Google Scholar 

  • Lu L, Yin S, Liu X, Zhang W, Gu T, Shen Q, Qiu H (2013) Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lou J, Yang L, Wang H, Wu L, Xu J (2018) Assessing soil bacterial community and dynamics by integrated high-throughput absolute abundance quantification. Peer J 6(3):e4514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mao ZS, Long YJ, Zhu YY, Zhu SS, He XH, Chen ZJ (2014) First report of Cylindrocarpon destructans var. destructans causing black root rot of Sanqi (Panax notoginseng) in China. Plant Dis 98:162–162

    Article  CAS  PubMed  Google Scholar 

  • Mi CY, Yang RH, Rao JF, Yang SZ, Wei FG, Li O, Hu XF (2017) Unveiling of dominant fungal pathogens associated with rusty root rot of Panax notoginseng based on multiple methods. Plant Dis 101:2046–2052

    Article  CAS  PubMed  Google Scholar 

  • Miao Z, Li S, Liu X, Chen Y, Li Y, Wang Y, Guo R, Xia Z, Zhang K (2006) The causal microorganisms of Panax notoginseng root rot disease. Sci Agr Sin 39:1371–1378

    Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Article  Google Scholar 

  • Pavón MÁ, González I, Martín R, Lacarra TG (2012) ITS-based detection and quantification of Alternaria spp. in raw and processed vegetables by real-time quantitative PCR. Food Microbiol 32:165–171

    Article  PubMed  CAS  Google Scholar 

  • Pavón MÁ, González I, Rojas M, Pegels N, Martín R, García T (2011) PCR detection of Alternaria spp. in processed foods, based on the internal transcribed spacer genetic marker. J Food Prot 74:240–247

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3–900051–07-0

  • Ren Y, Xun W, Yan H, Ma A, Xiong W, Shen Q, Zhang R (2020) Functional compensation dominates the assembly of plant rhizospheric bacterial community. Soil Biol Biochem 150:107968

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Zhang HC, Sun LG, Qi GF, Chen S, Zhao XY (2017) Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci Rep 7:343

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wen T, Yuan J, He XM, Lin Y, Huang QW, Shen QR (2020) Enrichment of beneficial cucumber rhizosphere microbes mediated by organic acid secretion. Hortic Res 7:154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Wu L, Wang J, Zhu Q, Lin S, Xu J, Zheng C, Chen J, Qin X, Fang C, Zhang Z, Azeem S, Lin W (2016) Mixed phenolic acids mediated proliferation of pathogens Talaromyces helicus and Kosakonia sacchari in continuously monocultured Radix pseudostellariae rhizosphere soil. Front Microbiol 7:335

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu H, Xia J, Qin X, Wu H, Lin W (2020) Underlying mechanism of wild Radix pseudostellariae in tolerance to disease under the natural forest cover. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.01142

  • Wu H, Xu J, Wang J, Qin X, Wu L, Li Z, Lin S, Lin W, Zhu Q, Khan MU, Lin W (2017) Insights into the mechanism of proliferation on the special microbes mediated by phenolic acids in the Radix pseudostellariae rhizosphere under continuous monoculture regimes. Front Plant Sci 8:659

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu L, Jie L, Wang W, Dai D, Cheng X, Zhang Z, Yang Y (2014) Identification and content determination of phenolic acids of rhizosphere soil of Panax notoginseng. Modernization Tradit Chi Med Mater Med-World Sci Technol 16:825–829

    Google Scholar 

  • Wu Z, Hao Z, Zeng Y, Guo L, Huang L, Chen B (2015a) Molecular characterization of microbial communities in the rhizosphere soils and roots of diseased and healthy Panax notoginseng. Antonie Leeuw 108:1059–1074

    Article  Google Scholar 

  • Wu Z, Hao Z, Zeng Y, Guo L, Huang L, Wang Y, Chen B (2015b) Molecular quantification of Cylindrocarpon destructans in the rhizosphere of Panax notoginseng for predicting plant. Microbiol China 42:598–607

    CAS  Google Scholar 

  • Ren X, Qin X, Wang M, Lei Z, Wang Y, Gao F (2016) Identification of dominant pathogen causing root rot disease in Astragalus membranaceus var. mongholicus of Shanxi Province and screening of antagonistic microorganism. J Chi Med Mater 39:2173–2177

    Google Scholar 

  • Xiong W, Li R, Ren Y, Liu C, Zhao Q, Wu H, Jousset A, Shen Q (2017) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207

    Article  CAS  Google Scholar 

  • Yang M, Zhang X, Xu Y, Mei X, Jiang B, Liao J, Yin Z, Zheng J, Zhao Z, Fan L, He X, Zhu Y, Zhu S (2015) Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 10(2):e0118555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao J, Ni T, Li Y, Xiong W, Ran W, Shen B, Shen Q, Zhang R (2014) Responses of bacterial communities in arable soils in a rice-wheat cropping system to different fertilizer regimes and sampling times. PLoS One 9:e85301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao J, Li Y, Wang B, Huang X, Yang L, Lan T, Zhang J, Cai Z (2017) Comparative soil microbial communities and activities in adjacent Sanqi ginseng monoculture and maize-Sanqi ginseng systems. Appl Soil Ecol 120:89–96

    Article  Google Scholar 

  • Zhao J, Ni T, Li J, Lu Q, Fang Z, Huang Q, Zhang R, Li R, Shen B, Shen Q (2016) Effects of organic–inorganic compound fertilizer with reduced chemical fertilizer application on crop yields, soil biological activity and bacterial community structure in a rice–wheat cropping system. Appl Soil Ecol 99:1–12

    Article  Google Scholar 

  • Zhao YM, Cheng YX, Ma YN, Chen CJ, Xu FR, Dong X (2018) Role of phenolic acids from the rhizosphere soils of Panax notoginseng as a double-edge sword in the occurrence of root-rot disease. Molecules 23:819

    Article  PubMed Central  CAS  Google Scholar 

  • Zheng YK, Miao CP, Chen HH, Huang FF, Xia YM, Chen YW, Zhao LX (2017) Endophytic fungi harbored in Panax notoginseng: diversity and potential as biological control agents against host plant pathogens of root-rot disease. J Gin Res 41:353–360

    Article  Google Scholar 

  • Zhou X, Zhang J, Pan D, Xin G, Wu F (2018) p-Coumaric can alter the composition of cucumber rhizosphere microbial communities and induce negative plant-microbial interactions. Biol Fert Soils 54:1–10

    CAS  Google Scholar 

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Acknowledgements

We also would like to thank the staffs in Miaoxiang Sanqi Technology Co., Ltd. for managing the field experiment and providing the convenience for sample collection.

Funding

This study was financially supported by the National Natural Science Foundation of China (42077031, 41701277), the China Postdoctoral Science Foundation (2018 M630573, 2019 T120442), the Reserve Talent Project of Young and Middle-aged Academic and Technical Leaders of Yunnan Province (202005 AC160043), and the Opening Project of Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control (NUEORS202002).

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Author notes

  1. Baoying Wang and Qing Xia contributed equally to this work.

Authors and Affiliations

  1. School of Geography, Nanjing Normal University, Nanjing, 210023, China

    Baoying Wang, Qing Xia, Yunlong Li, Jun Zhao, Xinqi Huang, Jinbo Zhang & Zucong Cai

  2. Jiangsu Engineering Research Center for Soil Utilization & Sustainable Agriculture, Nanjing, 210023, China

    Jun Zhao, Xinqi Huang, Jinbo Zhang & Zucong Cai

  3. Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and Application, Nanjing, 210023, China

    Jun Zhao & Zucong Cai

  4. Miaoxiang Sanqi Technology Co., Ltd., Wenshan County, 663000, China

    Shaozhou Yang & Fugang Wei

  5. Key Laboratory of Virtual Geographical Environment (Nanjing Normal University), Ministry of Education, Nanjing, 210023, China

    Jinbo Zhang & Zucong Cai

Authors
  1. Baoying Wang
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  2. Qing Xia
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  3. Yunlong Li
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  4. Jun Zhao
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Contributions

JZ, XQH, and ZCC conceived and designed research. BYW, QX, and YLL conducted experiments. BYW and JZ analyzed data and wrote the manuscript. JBZ, SZY, and FGW commented the manuscript. All authors read and approved the manuscript.

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Correspondence to Jun Zhao.

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Wang, B., Xia, Q., Li, Y. et al. Root rot-infected Sanqi ginseng rhizosphere harbors dynamically pathogenic microbiotas driven by the shift of phenolic acids. Plant Soil 465, 385–402 (2021). https://doi.org/10.1007/s11104-021-05034-4

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