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Ginsenosides in root exudates of Panax notoginseng drive the change of soil microbiota through carbon source different utilization

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Abstract

Background and aims

Ginsenosides are the main bioactive components of Panax plants which could be secreted by root and show autotoxicity to root cells or promote the growth of soil-borne pathogens. However, comprehensive understanding of the effect of ginsenosides on soil microbiota is still lacking.

Methods

The ginsenosides in root exudates of P. notoginseng were quantified and exogenous ginsenosides on soil microbiota were tested using 16S rRNA and ITS gene tag sequencing. Then its underlying mechanism was deciphered through studying effects of ginsenosides on growth of the ginsenoside-modified culturable fungi and bacteria as well as the relationships between these fungi and bacteria.

Results

Exogenous root exudates and mixtures of Rg1 + Rb1 + Rd had similar ability to drive the change of soil microbiota. Further studies demonstrated that Rg1 + Rb1 + Rd mixture could enrich or suppress special fungi and bacteria to modify soil community through differential utilization of carbon source during the early stage (30 days), followed by antagonism between ginsenoside-modified fungi and bacteria to determine soil microbial community modification at later stage (60 and 90 days).

Conclusions

Ginsenosides were the main substances in exogenous root exudates of P. notoginseng that drove the change in soil microbiota, mediating the special interaction between the plant and the microbiota.

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References

  • Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Plant Signal Behav 7:636–641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681

    CAS  PubMed  Google Scholar 

  • Badri DV, Chaparro JM, Zhang R, Shen Q, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19:90–98

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13

    CAS  Google Scholar 

  • Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

    CAS  PubMed  Google Scholar 

  • Berendsen RL, Vismans G, Yu K, Song Y, de Jonge R, Burgman WP, Burmølle M, Herschend J, Bakker PAHM, Pieterse CMJ (2018) Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–1507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    CAS  Google Scholar 

  • Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. PNAS 110:1621–1630.

  • Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl. Environ Microbiol 74:738–744

    CAS  Google Scholar 

  • Broughton WJ, Zhang F, Perret X, Staehelin C (2003) Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives. Plant Soil 252:129–137

    CAS  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol 64:807–838

    CAS  Google Scholar 

  • Cai T, Cai W, Zhang J, Zheng H, Tsou AM, Xiao L, Zhong Z, Zhu J (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol Microbiol 73:507–517.

  • Canarini A, Kaiser C, Merchant A, Richter A, Wanek W (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157

    PubMed  PubMed Central  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Google Scholar 

  • Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803

    CAS  PubMed  Google Scholar 

  • Chi K, Lei F, Xu Y, Liu F, Yang H, Zhang A, Zhang L (2016) Chemotaxis response of Fusarium solani and Cylindrocarpon destructans on total ginsenosides. Chinese herbal medicine 47:821–826

    CAS  Google Scholar 

  • Christensen LP (2009) Chapter 1 ginsenosides: chemistry, biosynthesis, analysis, and potential health effects. Adv Food Nutr 55:1–99

    CAS  Google Scholar 

  • Corral-Lugo A, Daddaoua A, Ortega A, Espinosa-Urgel M, Krell T (2016) Rosmarinic acid is a homoserine lactone mimic produced by plants that activates a bacterial quorum-sensing regulator. Sci Signal 9:ra1.

  • Cotton TEA, Petriacq P, Cameron DD, Meselmani MA, Schwarzenbacher R, Rolfe SA, Ton J (2019) Metabolic regulation of the maize rhizobiome by benzoxazinoids. ISME J 13:1647–1658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Court WA, Hendel JG, Elmi J (1996) Reversed-phase high-performance liquid chromatography determination of ginsenosides of Panax quinquefolium. J Chromatogr A 755:11–17

    CAS  Google Scholar 

  • DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178.

  • Dogan S, Günay H, Leyhausen G, Geurtsen W (2003) Effects of low-concentrated chlorhexidine on growth of Streptococcus sobrinus and primary human gingival fibroblasts. Clin Oral Investig 7:212–216

    CAS  PubMed  Google Scholar 

  • Fan B, Carvalhais LC, Becker A, Fedoseyenko D, von Wirén N, Borriss R (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol 12(1):116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frey-Klet P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol. Mol Biol Rev 75:583–609

    Google Scholar 

  • Fujioka N, Kohda H, Yamasaki K, Kasai R, Shoyama Y, Nishioka I (1989) Dammarane and oleanane saponins from callus tissue of Panax japonicus. Phytochemistry 28:1855–1858

    CAS  Google Scholar 

  • Gabriel-Ajobiewe RAO, Akinyele BJ, Mirrila EB (2012) Basal media formulation using Canavalia ensiformis as carbon and nitrogen source for the growth of some fungi species. J Microbiol Biotechnol Food Sci 1:1136–1151

    Google Scholar 

  • Goldford JE, Lu N, Bajić D, Estrela S, Mm T, Sanchez-Gorostiaga A, Segrè D, Mehta P, Sanchez A (2018) Emergent simplicity in microbial community assembly. Science 361:469–474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    CAS  Google Scholar 

  • Hassan S, Mathesius U (2012) The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot 63:3429–3444

    CAS  PubMed  Google Scholar 

  • Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, van der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2738

    PubMed  PubMed Central  Google Scholar 

  • Huang XF, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275

    Google Scholar 

  • Huang Y, Kuang Z, Wang W, Cao L (2016) Exploring potential bacterial and fungal biocontrol agents transmitted from seeds to sprouts of wheat. Biol Control 98:27–33

    Google Scholar 

  • Huang AC, Jiang T, Liu YX, Bai YC, Reed J, Qu B, Goossens A, Nützmann HW, Bai Y, Osbourn A (2019) A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364:eaau6389

    CAS  PubMed  Google Scholar 

  • Jia XH, Wang CQ, Liu JH, Li XW, Wang X, Shang MY, Cai SQ, Zhu S, Komatsu K (2013) Comparative studies of saponins in 1–3-year-old main roots, fibrous roots, and rhizomes of Panax notoginseng, and identification of different parts and growth-year samples. J Nat Med 67:339–349

    CAS  PubMed  Google Scholar 

  • Jiang JL, Yu M, Hou RP, Li L, Ren XM, Jiao CG, Yang LJ, 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

    CAS  Google Scholar 

  • Jiao XL, Bi W, Li M, Luo Y, Gao WW (2010) Dynamic response of ginsenosides in American ginseng to root fungal pathogens. Plant Soil 339:317–327

    Google Scholar 

  • Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant-Microbe Interact 14:775–784

    CAS  PubMed  Google Scholar 

  • Koprivova A, Schuck S, Jacoby RP, Klinkhammer I, Welter B, Leson L, Martyn A, Nauen J, Grabenhorst N, Mandelkow JF, Zuccaro A, Zeier J, Kopriva S (2019) Root-specific camalexin biosynthesis controls the plant growthpromoting effects of multiple bacterial strains. PNAS 116:15735–15744

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7.0: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  Google Scholar 

  • Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG, Dangl JL (2015) Plant microbiome. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864.

  • Legrand F, Picot A, Cobo-Díaz JF, Chen W, Le Floch G (2017) Challenges facing the biological control strategies for the management of Fusarium head blight of cereals caused by F. graminearum. Biol Control 113:26–38

    Google Scholar 

  • Lei FJ, Zhang AH, Xu YH, Zhang LX (2010) Allelopathic effects of ginsenosides on in vitro growth and antioxidant enzymes activity of ginseng callus. Allelopath J 26:13–22

    Google Scholar 

  • Li S, Du L, Yuen G, Harris SD (2006) Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 17:1218–1227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ying YX, Zhao DY, Ding WL (2012) Microbial community diversity analysis of Panax ginseng rhizosphere and non-rhizosphere soil using randomly amplified polymorphic DNA method. Open Journal of Genetics 2(2):95–102

    CAS  Google Scholar 

  • Liu XX, Hu X, Cao Y, Pang WJ, Huang JY, Guo P, Huang L (2019) Biodegradation of phenanthrene and heavy metal removal by acid-tolerant Burkholderia fungorum FM-2. Front Microbiol 10:408

    PubMed  PubMed Central  Google Scholar 

  • Luo LL, 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

    PubMed  PubMed Central  Google Scholar 

  • Lv H, Cao H, Nawaz MA, Sohail H, Huang Y, Cheng F, Kong Q, Bie Z (2018) Wheat intercropping enhances the resistance of watermelon to Fusarium wilt. Front Plant Sci 9:696

    PubMed  PubMed Central  Google Scholar 

  • Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS One 7(4):e35498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann G, George TS, Plassard C (2009) Strategies and methods for studying the rhizosphere-the plant science toolbox. Plant Soil 321:431–456

    CAS  Google Scholar 

  • Nicol RW, Traquair JA, Bernards MA (2002) Ginsenosides as host resistance factors in American ginseng (Panax quinquefolius). Can J Bot 80:557–562

    CAS  Google Scholar 

  • Nicol RW, Yousef L, Traquair JA, Bernards MA (2003) Ginsenosides stimulate the growth of soil borne pathogens of American ginseng. Phytochemistry 64:257–264

    CAS  PubMed  Google Scholar 

  • Osbourn AE (1996) Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8:1821–1831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci 110(16):6548–6553

    CAS  PubMed  Google Scholar 

  • Qi LW, Wang CZ, Yuan CS (2011) Ginsenosides from American ginseng: chemical and pharmacological diversity. Phytochemistry 72:689–699

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annu Rev Phytopathol 53:403–424

    CAS  PubMed  Google Scholar 

  • Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stringlis IA, Yu K, Feussner K, de Jonge R, Bentum SV, Verk MCV, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. PNAS 115:E5213–E5222

    CAS  PubMed  Google Scholar 

  • Sun WM, Ma YN, Yin YJ, Chen CJ, Xu FR, Dong X, Cheng YX (2018) Effects of essential oils from zingiberaceae plants on root-rot disease of Panax notoginseng. Molecules 23:1021–1032

    PubMed Central  Google Scholar 

  • Thimmappa R, Geisler K, Louveau T, O'maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257

    CAS  PubMed  Google Scholar 

  • Tran QL, Adnyana IK, Tezuka Y, Nagaoka T, Tran QK, Kadota S (2001) Triterpene saponins from Vietnamese ginseng (Panax vietnamensis) and their hepatocytoprotective activity. J Nat Prod 64:456–461

    CAS  PubMed  Google Scholar 

  • Turner EM (1956) The nature of the resistance of oats to the take-all fungus. J Exp Bot 4:264–271

    Google Scholar 

  • Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A, Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7(12):2248–2258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21:187–198

    CAS  PubMed  Google Scholar 

  • Wang RF, Zheng MM, Cao YD, Li H, Li CX, Xu JH, Wang ZT (2015) Enzymatic transformation of vina-ginsenoside R7 to rare notoginsenoside ST-4 using a new recombinant glycoside hydrolase from Herpetosiphon aurantiacus. Appl Microbiol Biotechnol 99:3433–3442

    CAS  PubMed  Google Scholar 

  • Wargo MJ, Hogan DA (2006) Fungal-bacterial interactions: a mixed bag of mingling microbes. Curr Opin Microbiol 9:359–364

    CAS  PubMed  Google Scholar 

  • Wei S, Wang Y, Li J, Zhang H, Ding L (2007) Investigation of ginsenosides in different parts and ages of Panax ginseng. Food Chem 102:664–668

    Google Scholar 

  • Xia P, Guo H, Mei R, Yang D, Liang Z, Yan X, Liu Y (2017) Accumulation of saponins in Panax notoginseng during its growing seasons. Ind Crop Prod 104:287–292

    CAS  Google Scholar 

  • Yang M, Zhang XD, Xu YG, Mei XY, Jiang BB, Liao JJ, Yin ZB, Zheng JF, Zhao Z, Fan LM, He XH, Zhu YY, Zhu SS (2015) Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 10:e0118555

    PubMed  PubMed Central  Google Scholar 

  • Yang M, Chuan YC, Guo CW, Liao JJ, Xu YG, Mei XY, Liu YX, Huang HC, He XH, Zhu SS (2018a) Panax notoginseng root cell death caused by the autotoxic ginsenoside Rg1 is due to over-accumulation of ROS, as revealed by transcriptomic and cellular approaches. Front Plant Sci 9:264

    PubMed  PubMed Central  Google Scholar 

  • Yang M, Duan SC, Mei XY, Huang HC, Chen W, Liu YX, Guo CW, Yang T, Wei W, Liu XL, He XH, Dong Y, Zhu SS (2018b) The Phytophthora cactorum genome provides insights into the adaptation to host defense compounds and fungicides. Sci Rep 8:6534

    PubMed  PubMed Central  Google Scholar 

  • Yang M, Yuan Y, Huang HC, Ye C, Guo CW, Xu YG, Wang WP, He XH, Liu YX, Zhu SS (2019) Steaming combined with biochar application eliminates negative plant-soil feedback for sanqi cultivation. Soil Tillage Res 189:189–198

    Google Scholar 

  • Ye J, Song Z, Wang L, Zhu J (2016) Metagenomic analysis of microbiota structure evolution in phytoremediation of a swine lagoon wastewater. Bioresour Technol 219:439–444

    CAS  PubMed  Google Scholar 

  • Yousef LF, Bernards MA (2006) In vitro metabolism of ginsenosides by the ginseng root pathogen Pythium irregulare. Phytochemistry 67:1740–1749

    CAS  PubMed  Google Scholar 

  • Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, Huang Q, Bai Y, Vivanco JM, Kowalchuk GA, Berendsen RL, Shen Q (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156

    PubMed  PubMed Central  Google Scholar 

  • Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, Cho H, Karaoz U, Loqué D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480

    CAS  PubMed  Google Scholar 

  • Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374(1):689–700

    CAS  Google Scholar 

  • Zhang RF, Vivanco JM, Shen QR (2017) The unseen rhizosphere root–soil–microbe interactions for crop production. Curr Opin Microbiol 37:8–14

    PubMed  Google Scholar 

  • Zhou JM, Cui XM, Zeng HC, Yang JZ, Ma N, Zhang WB, Zhu L (2009) Study on chemical composition of root exudates of Panax notoginseng. Special Wild Economic Animal and Plant Research 3:37–39

    CAS  Google Scholar 

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Acknowledgements

This work was partially funded by the National Key Research and Development Program of China (2017YFD0201601-5 and 2017YFC1702502), the Natural Science Foundation of China (31772404 and 31660605), the Young and Middle-aged Academic and Technical Leaders Reserve Programme in Yunnan Province (2017HB024), the Yunnan Ten Thousand Talents Plan Young & Elite Talents Project, the Yunnan Academician Workstation of Chinese Academy of Engineering (2018IC063), Yunnan provincial key programs of Yunnan Eco-friendly Food International Cooperation Research Center project under grant 2019ZG00901 and Program for Innovative Research Team in Science and Technology in University of Yunnan Province.

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Luo, LF., Yang, L., Yan, ZX. et al. Ginsenosides in root exudates of Panax notoginseng drive the change of soil microbiota through carbon source different utilization. Plant Soil 455, 139–153 (2020). https://doi.org/10.1007/s11104-020-04663-5

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