Skip to main content
SpringerLink
Log in

Diversity and antifungal activity of endophytic bacteria associated with Panax ginseng seedlings

  • Short Communication
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Ginseng (Panax ginseng C.A. Meyer) is a medicinal crop that requires a long culture time before it is ready to harvest, thus generating high economic and environmental costs. Symbiotic bacteria that live within the plant provide the host plant with many advantages in terms of metabolism and disease resistance. Here, we isolated endophytic bacteria from various tissues of P. ginseng seedlings using a culture-dependent method and we compared their tissue distribution. In addition, their antimicrobial activity against two fungal pathogens was investigated. Based on 16S rRNA sequencing, we identified 21 bacterial strains from ginseng seedlings. Leaves and rhizomes showed higher bacterial species diversity than root bodies and tails. While Bacillus strains were detected in all tissues, Xanthomonas and Micrococcaceae strains were specifically isolated from rhizome and leaf tissues, respectively. Fourteen bacterial strains showed antimicrobial activities against Cylindrocarpon destructans and/or Botrytis cinerea, with different activities. Among them, two strains (PgKB29 and PgKB35) showed strong antimicrobial activities against both fungi. Taken together, these results provide a better understanding of endophytic bacteria in P. ginseng seedlings and suggest the possibility of biological control of fungal pathogens using endophytic bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Andreolli M, Lampis S, Zapparoli G, Angelini E, Vallini G (2016) Diversity of bacterial endophytes in 3 and 15 year-old grapevines of Vitis vinifera cv. Corvina and their potential for plant growth promotion and phytopathogen control. Microbiol Res 183:42–52

    Article  Google Scholar 

  • Ben Rejeb I, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants 3:458–475

    Article  CAS  Google Scholar 

  • Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS One 8(2):e56329

    Article  CAS  Google Scholar 

  • Borriss R, Chen XH, Rueckert C, Blom J, Becker A, Baumgarth B, Fan B, Pukall R, Schumann P, Sproer C, Junge H, Vater J, Puhler A, Klenk HP (2011) Relationship of Bacillus amyloliquefaciens clades associated with strains DSM7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. Int J Syst Evol Microbiol 61:1786–1801

    Article  CAS  Google Scholar 

  • Brader G, Gompant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    Article  CAS  Google Scholar 

  • Card S, Johnson L, Teasdale S, Caradus J (2016) Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiol Ecol 92:fiw114

    Article  Google Scholar 

  • Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, Sa T (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8:705

    Article  Google Scholar 

  • Chen XH, Vater J, Piel J, Franke P, Scholz R, Schneider K, Koumoutsi A, Hitzeroth G, Grammel N, Strittmatter AW, Gottschalk G, Sussmuth RD, Borriss R (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188:4024–4036

    Article  CAS  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  Google Scholar 

  • Cho H-S, Jeon Y-H, Do G-R, Cho D-H, Yu Y-H (2008) Mycological characteristics of Botrytis cinerea causing gray mold on ginseng in Korea. J Ginseng Res 32:26–32

    Article  Google Scholar 

  • Choi KT (2008) Botanical characteristics, pharmacological effects and medicinal components of Korean Panax ginseng C A Meyer. Acta Pharmacol Sin 29:1109–1118

    Article  CAS  Google Scholar 

  • Chowdhury SP, Hartmann A, Gao X, Borriss R (2015) Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42—a review. Front Microbiol 6:780

    Article  Google Scholar 

  • Compant S, Brader G, Muzammil S, Sessitsch A, Lebrihi A, Mathieu F (2013) Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. BioControl 58(4):435–455

    Article  Google Scholar 

  • Dayeon K, Byung-Yong K, Jae-Hyung A, Hang-Yeon W, Sung-Il K, Wan-Gyu K, Jaekyeong S (2015) Quantitative analysis of Bacillus amyloliquefaciens GR4-5 in soil. Korean J Organic 23:847–858

    Article  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 Ginseng Res 42:9–15

    Article  Google Scholar 

  • Gao Y, Liu Q, Zang P, Li X, Ji Q, He Z, Zhao Y, Yang H, Zhao X, Zhang L (2015) An endophytic bacterium isolated from Panax ginseng C.A. Meyer enhances growth, reduces morbidity, and stimulates ginsenoside biosynthesis. Phytochem Lett 11:132–138

    Article  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, Berg G, Pirttila AM, Compant S, Campisano A, Doring M, Sessitsch A (2015) The Hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  Google Scholar 

  • Hong CE, Jo SH, Moon JY, Lee J-S, Kwon S-Y, Park JM (2015) Isolation of novel leaf-inhabiting endophytic bacteria in Arabidopsis thaliana and their antagonistic effects on phytophathogens. Plant Biotechnol Rep 9:451–458

    Article  Google Scholar 

  • Hong CE, Kwon SY, Park JM (2016) Biocontrol activity of Paenibacillus polymyxa AC-1 against Pseudomonas syringae and its interaction with Arabidopsis thaliana. Microbiol Res 185:13–21

    Article  CAS  Google Scholar 

  • Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201

    Article  CAS  Google Scholar 

  • Iniguez AL, Dong Y, Carter HD, Ahmer BMM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. MPMI 18:169–178

    Article  CAS  Google Scholar 

  • Jo IH, Lee SH, Kim YC, Kim DH, Kim HS, Kim KH, Chung JW, Bang KH (2015) De novo transcriptome assembly and the identification of gene-associated single-nucleotide polymorphism markers in Asian and American ginseng roots. Mol Genet Genom 290:1055–1065

    Article  CAS  Google Scholar 

  • Chowdhury E, Jeon J, Ok Rim S, Park Y-H, Kyu Lee S, Bae H (2017) Composition, diversity and bioactivity of culturable bacterial endophytes in mountain-cultivated ginseng in Korea. Sci Rep 7:10098

    Article  Google Scholar 

  • Kim IJ, Park SJ, Nam SY, Choi Y, Lee C-S, Yun CK, Lee JS, Shin SG (2012) Comparison of labor-saving and economical efficiency on mechanical transplants of ginseng seedling. J Korean Soc Int Agric 24:203–206

    Google Scholar 

  • Lee JS, Han KS, Lee SC, Soh JW, Kim DW (2014) Environmental factors on the development of root rot on ginseng caused by Cylindrocarpon destructans. Res Plant Dis 20:87–94

    Article  Google Scholar 

  • Lee JH, Lee JS, Kwon WS, Kang JY, Lee DY, In JG, Kim YS, Seo J, Baeg IH, Chang IM, Grainger K (2015) Characteristics of Korean ginseng varieties of Gumpoong, Sunun, Sunpoong, Sunone, Cheongsun, and Sunhyang. J Ginseng Res 39:94–104

    Article  Google Scholar 

  • Leung KW, Wong AS (2010) Pharmacology of ginsenosides: a literature review. Chin Med 5:20

    Article  Google Scholar 

  • Li Y, Zhao D, Ding W, Ying Y (2012) Isolation of endophytic bacteria in roots of Panax ginseng and screening of antagonistic strains against phytopathogens prevalent in P. ginseng. Zhongguo Zhong Yao Za Zhi 37:1532–1535

    PubMed  Google Scholar 

  • Li H, Soares MA, Torres MS, Bergen M, White JF (2015) Endophytic bacterium, Bacillus amyloliquefaciens, enhances ornamental hosta resistance to diseases and insect pests. J Plant Interact 10:224–229

    Article  CAS  Google Scholar 

  • Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552

    Article  Google Scholar 

  • Luo H, Sun C, Sun Y, Wu Q, Li Y, Song J, Niu Y, Cheng X, Xu H, Li C, Liu J, Steinmetz A, Chen S (2011) Analysis of the transcriptome of Panax notoginseng root uncovers putative triterpene saponin-biosynthetic genes and genetic markers. BMC Genom 12(Suppl 5):S5

    Article  CAS  Google Scholar 

  • Ma L, Cao YH, Cheng MH, Huang Y, Mo MH, Wang Y, Yang JZ, Yang FX (2013) Phylogenetic diversity of bacterial endophytes of Panax notoginseng with antagonistic characteristics towards pathogens of root-rot disease complex. Antonie Van Leeuwenhoek 103:299–312

    Article  Google Scholar 

  • Oliynyk S, Oh S (2013) Actoprotective effect of ginseng: improving mental and physical performance. J Ginseng Res 37:144–166

    Article  CAS  Google Scholar 

  • Park YD, Lee HB, Yi H, Kim Y, Bae KS, Choi JE, Jung HS, Chun J (2005) Pseudomonas panacis sp. nov., isolated from the surface of rusty roots of Korean ginseng. Int J Syst Evol Microbiol 55:1721–1724

    Article  CAS  Google Scholar 

  • Park YH, Lee SG, Ahn DJ, Kwon TR, Park SU, Lim HS, Bae H (2012) Diversity of fungal endophytes in various tissues of Panax ginseng Meyer cultivated in Korea. J Ginseng Res 36:211–217

    Article  Google Scholar 

  • Paulin MM, Novinscak A, St-Arnaud M, Goyer C, DeCoste NJ, Prive JP, Owen J, Filion M (2009) Transcriptional activity of antifungal metabolite-encoding genes phlD and hcnBC in Pseudomonas spp. using qRT-PCR. FEMS Microbiol Ecol 68:212–222

    Article  CAS  Google Scholar 

  • Prakash O, Nimonkar Y, Munot H, Sharma A, Vemuluri VR, Chavadar MS, Shouche YS (2014) Description of Micrococcusaloeverae sp. nov., an endophytic actinobacterium isolated from Aloe vera. Int J Syst Evol Microbiol 64:3427–3433

    Article  Google Scholar 

  • Rahman M, Punja ZK (2005) Factors influencing development of root rot on ginseng caused by Cylindrocarpon destructans. Phytopathology 95:1381–1390

    Article  Google Scholar 

  • Romero FM, Marina M, Pieckenstain FL (2014) The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Microbiol Lett 187:187–194

    Article  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. MPMI 19:827–837

    Article  CAS  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  Google Scholar 

  • Soares MA, Li H-Y, Bergen M, da Silva JM, Kowalski KP, White JF (2016) Functional role of an endophytic Bacillus amyloliquefaciens in enhancing growth and disease protection of invasive English ivy (Hedera helix L.). Plant Soil 405:107–123

    Article  CAS  Google Scholar 

  • Song M, Yun HY, Kim YH (2014) Antagonistic Bacillus species as a biological control of ginseng root rot caused by Fusarium cf. incarnatum. J Ginseng Res 38:136–145

    Article  Google Scholar 

  • Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48:559–565

    Article  CAS  Google Scholar 

  • Verhagen BW, Trotel-Aziz P, Couderchet M, Hofte M, Aziz A (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260

    Article  CAS  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214

    Article  CAS  Google Scholar 

  • Zouari I, Jlaiel L, Tounsi S, Trigui M (2016) Biocontrol activity of the endophytic Bacillus amyloliquefaciens strain CEIZ-11 against Pythium aphanidermatum and purification of its bioactive compounds. Biol Control 100:54–62

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was carried out with the support of the KRIBB initiative program funded by the Ministry of Science and ICT (grant to J.M.P.).

Author information

Author notes

  1. Chi Eun Hong and Sung Hee Jo contributed equally to this work as first authors.

Authors and Affiliations

  1. Department of Herbal Crop Research, National Institute of Horticultural and Herbal Science (NIHHS), Rural Development Administration (RDA), Eumseong, 27709, South Korea

    Chi Eun Hong & Ick-Hyun Jo

  2. Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, 34141, South Korea

    Sung Hee Jo & Jeong Mee Park

  3. Department of Biosystems and Bioengineering, KRIBB School of Biotechnology, Korea University of Science and Technology (UST), Daejeon, 34113, South Korea

    Sung Hee Jo & Jeong Mee Park

Authors
  1. Chi Eun Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sung Hee Jo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ick-Hyun Jo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeong Mee Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ick-Hyun Jo or Jeong Mee Park.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hong, C.E., Jo, S.H., Jo, IH. et al. Diversity and antifungal activity of endophytic bacteria associated with Panax ginseng seedlings. Plant Biotechnol Rep 12, 409–418 (2018). https://doi.org/10.1007/s11816-018-0504-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-018-0504-9

Keywords

Search

Navigation