Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Rhizospheric fungi of Panax notoginseng: diversity and antagonism to host phytopathogens

  • Miao, Cui-Ping (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Mi, Qi-Li (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Qiao, Xin-Guo (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Zheng, You-Kun (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Chen, You-Wei (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Xu, Li-Hua (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Guan, Hui-Lin (School of Energy and Environment Science, Yunnan Normal University) ;
  • Zhao, Li-Xing (Key Laboratory of Microbial Diversity in Southwest China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University)
  • Received : 2015.01.12
  • Accepted : 2015.06.14
  • Published : 2016.04.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Rhizospheric fungi play an essential role in the plantesoil ecosystem, affecting plant growth and health. In this study, we evaluated the fungal diversity in the rhizosphere soil of 2-yr-old healthy Panax notoginseng cultivated in Wenshan, China. Methods: Culture-independent Illumina MiSeq and culture-dependent techniques, combining molecular and morphological characteristics, were used to analyze the rhizospheric fungal diversity. A diffusion test was used to challenge the phytopathogens of P. notoginseng. Results: A total of 16,130 paired-end reads of the nuclear ribosomal internal transcribed spacer 2 were generated and clustered into 860 operational taxonomic units at 97% sequence similarity. All the operational taxonomic units were assigned to five phyla and 79 genera. Zygomycota (46.2%) and Ascomycota (37.8%) were the dominant taxa; Mortierella and unclassified Mortierellales accounted for a large proportion (44.9%) at genus level. The relative abundance of Fusarium and Phoma sequenceswas high, accounting for 12.9% and 5.5%, respectively. In total,113 fungal isolates were isolated from rhizosphere soil. They were assigned to five classes, eight orders (except for an Incertae sedis), 26 genera, and 43 species based on morphological characteristics and phylogenetic analysis of the internal transcribed spacer. Fusarium was the most isolated genus with six species (24 isolates, 21.2%). The abundance of Phoma was also relatively high (8.0%). Thirteen isolates displayed antimicrobial activity against at least one test fungus. Conclusion: Our results suggest that diverse fungi including potential pathogenic ones exist in the rhizosphere soil of 2-yr-old P. notoginseng and that antagonistic isolates may be useful for biological control of pathogens.

Keywords

References

  1. Bouffaud ML, Kyselkova M, Gouesnard B, Grunamann G, Muller D, Moenne-Loccoz Y. Is diversification history of maize influencing selection of soil bacteria by roots? Mol Ecol 2012;21:195-206. https://doi.org/10.1111/j.1365-294X.2011.05359.x
  2. Xu L, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M. Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Boil Biochem 2012;46:26-32. https://doi.org/10.1016/j.soilbio.2011.11.010
  3. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 2013;37:634-63. https://doi.org/10.1111/1574-6976.12028
  4. Singh AK, Singh M, Dubey SK. Rhizospheric fungal community structure of a Bt brinjal and a near isogenic variety. J Appl Microbiol 2014;117:750-65. https://doi.org/10.1111/jam.12549
  5. Kristin A, Miranda H. The root microbiotada fingerprint in the soil? Plant Soil 2013;370:671-86. https://doi.org/10.1007/s11104-013-1647-7
  6. Lakshmanan V, Selvaraj G, Bais HP. Functional soil microbiome: belowground solutions to an aboveground problem. Plant Physiol 2014;166:689-700. https://doi.org/10.1104/pp.114.245811
  7. Aira M, Gomez-Brandon M, Lazcano C, Baath E, Dominguez J. Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 2010;42:2276-81. https://doi.org/10.1016/j.soilbio.2010.08.029
  8. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci 2012;17:478-86. https://doi.org/10.1016/j.tplants.2012.04.001
  9. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dang JL, Buckler ES, Ley RE. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 2013;110:6548-53. https://doi.org/10.1073/pnas.1302837110
  10. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 2009;184:449-56. https://doi.org/10.1111/j.1469-8137.2009.03003.x
  11. Sugiyama A, Ueda Y, Takase H, Yazaki K. Pyrosequencing assessment of rhizosphere fungal communities from a soybean field. Can J Microbiol 2014;60:687-90. https://doi.org/10.1139/cjm-2014-0443
  12. Gomes NC, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendona-Hagler L, Smalla K. Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 2003;69:3758-66. https://doi.org/10.1128/AEM.69.7.3758-3766.2003
  13. Rincon-Florez VA, Carvalhais LC, Schenk PM. Culture-independent molecular tools for soil and rhizosphere microbiology. Diversity 2013;5:581-612. https://doi.org/10.3390/d5030581
  14. Aravindraja C, Viszwapriya D. Karutha Pandian S. Ultra deep 16S rRNA sequencing analysis of geographically similar but diverse unexplored marine samples reveal varied bacterial community composition. PLOS One 2013;8:e76724. https://doi.org/10.1371/journal.pone.0076724
  15. Schmidt PA, Balint M, Greshake B, Bandow C, Rombk J, Schmitt I. Illumina metabarcoding of a soil fungal community. Soil Biol Biochem 2013;65:128-32. https://doi.org/10.1016/j.soilbio.2013.05.014
  16. Arumugam R, Chan XY, Yin WF, Choo SW, Chan KG. Metagenomic analysis of microbial diversity of tropical sea water of Georgetown Coast, Malaysia. Life Sci J 2013;1:2392-6.
  17. Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2014;2:6. https://doi.org/10.1186/2049-2618-2-6
  18. Sun HX, Ye YP, Pan HJ, Pan YJ. Adjuvant effect of Panax notoginseng saponins on the immune responses to ovalbumin in mice. Vaccine 2004;22:3882-9. https://doi.org/10.1016/j.vaccine.2004.04.012
  19. Guo HB, Cui XM, An N, Cai GP. Sanchi ginseng (Panax notoginseng (Burkill) F. H. Chen) in china: distribution, cultivation and variations. Genet Resour Crop Evol 2010;57:453-60. https://doi.org/10.1007/s10722-010-9531-2
  20. Ma L, Cao YH, Cheng MH, Huang Y, Mo MH, Wang Y, Yang JZ, Yang FX. Phylogenetic diversity of bacterial endophytes of Panax notoginseng with antagonistic characteristics towards pathogens of root-rot disease complex. Antonie van Leeuwenhoek 2013;103:299-312. https://doi.org/10.1007/s10482-012-9810-3
  21. Sun Y, Ke J, Ma N, Chen Z, Wang C, Cui X. Effects of root rot on saponin content in Panax notoginseng. Zhong Yao Cai 2004;27:79-80.
  22. Miao ZQ, Li SD, Liu XZ, Chen YJ, Li YH, Wang Y, Xia ZY, Zhang KQ. The causal microorganisms of Panax notoginseng root rot disease. Sci Agric Sin 2006;39:1371-8.
  23. Park YH, Kim YC, Park SU, Lim HS, Kim JB, Cho BK, Bae H. Age-dependent distribution of fungal endophytes in Panax ginseng roots cultivated in Korea. J Ginseng Res 2012;36:327-33. https://doi.org/10.5142/jgr.2012.36.3.327
  24. Eo JK, Choi MS, Eom AH. Diversity of endophytic fungi isolated from Korean ginseng leaves. Mycobiology 2014;42:147-51. https://doi.org/10.5941/MYCO.2014.42.2.147
  25. Xing X, Guo S, Fu J. Biodiversity and distribution of endophytic fungi associated with Panax quinquefolium L. cultivated in a forest reserve. Symbiosis 2010;51:161-6. https://doi.org/10.1007/s13199-010-0062-6
  26. Punja ZK. Fungal pathogens of American ginseng (Panax quinquefolium) in British Columbia. Can J Plant Pathol 1997;19:301-6. https://doi.org/10.1080/07060669709500528
  27. Chen X, Sun XD, Bi SY, Lu GZ. Fungi diversity of ginseng rhizosphere soil in northeastern China. Agric Sci Technol Hunan 2010;11:132-6.
  28. Ihrmark K, Bödeker IT, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-Durling M, Clemmensen KE, et al. New primers to amplify the fungal ITS2 regiondevaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 2012;8:2666-77.
  29. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537-41. https://doi.org/10.1128/AEM.01541-09
  30. Chao A, Chazdon RL, Colwell RK, Shen TJ. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 2005;8:148-59.
  31. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed- Mohideen AS, McGarrell DM, Marsh T, Garrity GM, et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009;37:D141-5. https://doi.org/10.1093/nar/gkn879
  32. Guo LD, Hyde KD, Liew ECY. Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 2000;147:617-30. https://doi.org/10.1046/j.1469-8137.2000.00716.x
  33. White TJ, Bruns T, Lee J, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego, CA, USA: Academic Press; 1990. p. 315-22.
  34. Monard C, Gantner S, Stenlid J. Utilizing ITS1 and ITS2 to study environmental fungal diversity using pyrosequencing. FEMS Microbiol Ecol 2013;84:165-75. https://doi.org/10.1111/1574-6941.12046
  35. Luo C, Tsementzi D, Kyrpides N, Read T, Konstantinidis KT. Direct comparisons of Illumina vs. Roche 454 sequencing technologies on the same microbial community DNA sample. PLoS One 2012;7:e30087. https://doi.org/10.1371/journal.pone.0030087
  36. Snelling TJ, Genç B, McKain N, Watson M, Waters SM, Creevey CJ, Wallace RJ. Diversity and community composition of methanogenic archaea in the rumen of Scottish upland sheep assessed by different methods. PLoS One 2014;9:e106491. https://doi.org/10.1371/journal.pone.0106491
  37. Wang Z, Yang Y, He T, Xie S. Change of microbial community structure and functional gene abundance in nonylphenol-degrading sediment. Appl Microbiol Biotechnol 2015;99:3259-68. https://doi.org/10.1007/s00253-014-6222-5
  38. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012;6:1621-4. https://doi.org/10.1038/ismej.2012.8
  39. Curlevski NJA, Xu ZH, Anderson IC, Cairney JWG. Diversity of soil and rhizosphere fungi under Araucaria bidwillii (Bunya pine) at an Australian tropical montane rainforest site. Fungal Divers 2010;40:12-22. https://doi.org/10.1007/s13225-009-0001-0
  40. Bazzicalupo AL, Balint M, Schmitt I. Comparison of ITS1 and ITS2 rDNA in 454 sequencing of hyperdiverse fungal communities. Fungal Ecol 2013;6:102-9. https://doi.org/10.1016/j.funeco.2012.09.003
  41. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Consortium FB. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 2012;109:6241-6. https://doi.org/10.1073/pnas.1117018109
  42. Jumpponen A, Jones KL. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 2009;184:438-48. https://doi.org/10.1111/j.1469-8137.2009.02990.x
  43. Cordier T, Robin C, Capdevielle X, Desprez-Loustau ML, Vacher C. Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica). Fungal Ecol 2012;5:509-20. https://doi.org/10.1016/j.funeco.2011.12.004
  44. De Azevedo Santiago AL, Dos Santos PJ, Maia LC. Mucorales from the semiarid of Pernambuco, Brazil. Braz J Microbiol 2013;44:299-305. https://doi.org/10.1590/S1517-83822013005000027
  45. Liu K, Zheng YK, Miao CP, Xiong ZJ, Xu LH, Guan HL, Yang YB, Zhao LX. The antifungal metabolites obtained from the rhizospheric Aspergillus sp. YIM PH30001 against pathogenic fungi of Panax notoginseng. Nat Prod Res 2014;28:2334-7. https://doi.org/10.1080/14786419.2014.935941
  46. Yan XR, Fu JF. A summary of researches on Cylindrocarpon and Panax root rust-rot. J Shenyang Agric Univ 2002;33:71-5.
  47. Bai RL, Liu XM, Liu WC. The fungal species causing root rot of ginseng in Jilin Province. Acta Phytopathol Sin 1999;29:285.
  48. U'Ren JM, Riddle JM, Monacell JT, Carbone I, Miadlikowska J, Aronold AE. Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Mol Ecol Resour 2014;14:1032-48.
  49. Lynch J. The rhizosphere. London, UK: Wiley; 1990.
  50. Haichar FZ, Santaella C, Heullin T, Achouak W. Root exudates mediated interactions belowground. Soil Biol Biochem 2014;77:69-80. https://doi.org/10.1016/j.soilbio.2014.06.017
  51. Yu C, Hu XM, Deng W, Li Y, Xiong C, Ye CH, Han GM, Li X. Changes in soil microbial community structure and functional diversity in the rhizosphere surrounding mulberry subjected to long-term fertilization. Appl Soil Ecol 2014;86:30-40.
  52. Schmitt H, Van Beelen P, Tolls J, Van Leeuwen CL. Pollution-induced community tolerance of soil microbial communities caused by the antibiotic sulfachloropyridazine. Environ Sci Technol 2004;38:1148-53. https://doi.org/10.1021/es034685p
  53. Thiele-Bruhn S, Beck IC. Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 2005;59:457-65. https://doi.org/10.1016/j.chemosphere.2005.01.023

Cited by

  1. Microbial Profiling of a Suppressiveness-Induced Agricultural Soil Amended with Composted Almond Shells vol.7, pp.None, 2016, https://doi.org/10.3389/fmicb.2016.00004
  2. High-throughput sequencing-based analysis of endogenetic fungal communities inhabiting the Chinese Cordyceps reveals unexpectedly high fungal diversity vol.6, pp.None, 2016, https://doi.org/10.1038/srep33437
  3. Rhizospheric microbial communities associated with wild and cultivated frankincense producing Boswellia sacra tree vol.12, pp.10, 2016, https://doi.org/10.1371/journal.pone.0186939
  4. Effects of cover crop in an apple orchard on microbial community composition, networks, and potential genes involved with degradation of crop residues in soil vol.54, pp.6, 2016, https://doi.org/10.1007/s00374-018-1298-1
  5. Identification of certain Panax species to be potential substitutes for Panax notoginseng in hemostatic treatments vol.134, pp.None, 2016, https://doi.org/10.1016/j.phrs.2018.05.005
  6. Soil fungal biodiversity and pathogen identification of rotten disease in Aconitum carmichaelii (Fuzi) roots vol.13, pp.10, 2016, https://doi.org/10.1371/journal.pone.0205891
  7. Diversity and bioactive potential of culturable fungal endophytes of Dysosma versipellis ; a rare medicinal plant endemic to China vol.8, pp.None, 2018, https://doi.org/10.1038/s41598-018-24313-2
  8. Monitoring Antifungal Agents of Artemisia annua against Fusarium oxysporum and Fusarium solani , Associated with Panax notoginseng Root-Rot Disease vol.24, pp.1, 2019, https://doi.org/10.3390/molecules24010213
  9. Negative Plant-Soil Feedback Driven by Re-assemblage of the Rhizosphere Microbiome With the Growth of Panax notoginseng vol.10, pp.None, 2016, https://doi.org/10.3389/fmicb.2019.01597
  10. Mycorrhizal Colonization and Soil Parameters Affected by Foliar Endophytes in Jatropha curcas L. vol.19, pp.2, 2016, https://doi.org/10.1007/s42729-019-00033-y
  11. The beneficial use of essential oils from buds and fruit of Syzygium aromaticum to combat pathogenic fungi of Panax notoginseng vol.133, pp.None, 2016, https://doi.org/10.1016/j.indcrop.2019.03.029
  12. Different Age-Induced Changes in Rhizosphere Microbial Composition and Function of Panax ginseng in Transplantation Mode vol.11, pp.None, 2020, https://doi.org/10.3389/fpls.2020.563240
  13. Diversity of rhizosphere and endophytic fungi in Atractylodes macrocephala during continuous cropping vol.8, pp.None, 2016, https://doi.org/10.7717/peerj.8905
  14. Citizen science project reveals high diversity in Didymellaceae ( Pleosporales , Dothideomycetes ) vol.65, pp.None, 2016, https://doi.org/10.3897/mycokeys.65.47704
  15. Autotoxic Ginsenoside Disrupts Soil Fungal Microbiomes by Stimulating Potentially Pathogenic Microbes vol.86, pp.9, 2016, https://doi.org/10.1128/aem.00130-20
  16. First Report on Lophiostoma macrostomum and Pestalotiopsis lespedezae Isolated from Conifer Leaves of Pinus densiflora in Korea vol.48, pp.2, 2016, https://doi.org/10.4489/kjm.20200013
  17. Biological Activities of Two Essential Oils from Pogostemon cablin and Eupatorium fortunei and Their Major Components against Fungi Isolated from Panax notoginseng vol.17, pp.12, 2020, https://doi.org/10.1002/cbdv.202000520
  18. Determination of the microbial communities of Guizhou Suantang, a traditional Chinese fermented sour soup, and correlation between the identified microorganisms and volatile compounds vol.138, pp.2, 2016, https://doi.org/10.1016/j.foodres.2020.109820
  19. Response of soil fungal communities to continuous cropping of flue-cured tobacco vol.10, pp.1, 2016, https://doi.org/10.1038/s41598-020-77044-8
  20. Effects of Fertilization Methods on Chemical Properties, Enzyme Activity, and Fungal Community Structure of Black Soil in Northeast China vol.12, pp.12, 2016, https://doi.org/10.3390/d12120476
  21. The influence of rhizosphere soil fungal diversity and complex community structure on wheat root rot disease vol.9, pp.None, 2016, https://doi.org/10.7717/peerj.12601
  22. Myrothins A–F from Endophytic Fungus Myrothecium sp. BS‐31 Harbored in Panax notoginseng vol.18, pp.3, 2016, https://doi.org/10.1002/cbdv.202000964
  23. Soil and microbe interactions in two populations of Appalachian black cohosh (Actaea racemosa L.)1 vol.148, pp.2, 2021, https://doi.org/10.3159/torrey-d-20-00026.1
  24. Impact of rhizosphere microorganisms on arsenic (As) transformation and accumulation in a traditional Chinese medical plant vol.28, pp.43, 2016, https://doi.org/10.1007/s11356-021-14500-6
  25. Antagonistic activity and characterization of indigenous soil isolates of bacteria and fungi against onion wilt incited by Fusarium sp. vol.204, pp.1, 2022, https://doi.org/10.1007/s00203-021-02663-2
  26. Dynamic changes in rhizosphere fungi in different developmental stages of wheat in a confined and isolated environment vol.106, pp.1, 2016, https://doi.org/10.1007/s00253-021-11698-w