Journal of Ginseng Research

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

DOI QR Code

Endophytic Trichoderma gamsii YIM PH30019: a promising biocontrol agent with hyperosmolar, mycoparasitism, and antagonistic activities of induced volatile organic compounds on root-rot pathogenic fungi of Panax notoginseng

  • Chen, Jin-Lian (School of Energy and Environment Science, Yunnan Normal University) ;
  • Sun, Shi-Zhong (School of Energy and Environment Science, Yunnan Normal University) ;
  • Miao, Cui-Ping (Key Laboratory of Microbial Diversity in South West China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University) ;
  • Wu, Kai (School of Energy and Environment Science, Yunnan Normal University) ;
  • Chen, You-Wei (Key Laboratory of Microbial Diversity in South West 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 South West 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 South West China of Ministry of Education and Laboratory for Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University)
  • Received : 2015.06.24
  • Accepted : 2015.09.25
  • Published : 2016.10.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Biocontrol agents are regarded as promising and environmental friendly approaches as agrochemicals for phytodiseases that cause serious environmental and health problems. Trichoderma species have been widely used in suppression of soil-borne pathogens. In this study, an endophytic fungus, Trichoderma gamsii YIM PH30019, from healthy Panax notoginseng root was investigated for its biocontrol potential. Methods: In vitro detached healthy roots, and pot and field experiments were used to investigate the pathogenicity and biocontrol efficacy of T. gamsii YIM PH30019 to the host plant. The antagonistic mechanisms against test phytopathogens were analyzed using dual culture, scanning electron microscopy, and volatile organic compounds (VOCs). Tolerance to chemical fertilizers was also tested in a series of concentrations. Results: The results indicated that T. gamsii YIM PH30019 was nonpathogenic to the host, presented appreciable biocontrol efficacy, and could tolerate chemical fertilizer concentrations of up to 20%. T. gamsii YIM PH30019 displayed antagonistic activities against the pathogenic fungi of P. notoginseng via production of VOCs. On the basis of gas chromatography-mass spectrometry, VOCs were identified as dimethyl disulfide, dibenzofuran, methanethiol, ketones, etc., which are effective ingredients for antagonistic activity. T. gamsii YIM PH30019 was able to improve the seedlings' emergence and protect P. notoginseng plants from soil-borne disease in the continuous cropping field tests. Conclusion: The results suggest that the endophytic fungus T. gamsii YIM PH30019 may have a good potential as a biological control agent against notoginseng phytodiseases and can provide a clue to further illuminate the interactions between Trichoderma and phytopathogens.

Keywords

References

  1. Dong TTX, Cui XM, Song ZH, Zhao KJ, Ji ZN, Lo CK, Tsim KWK. Chemical assessment of roots of Panax notoginseng in China: regional and seasonal variations in its active constituents. J Agric Food Chem 2013;51:4617-23.
  2. You CM, Chen XB, Tu W, Lou Q, Guan HL, Xie J. Theoretical thinking about Panax notoginseng's no-tillage cropping soil barriers and mitigation measures. J Yunnan Normal Univ 2010;30:44-8 [in Chinese].
  3. Wan JB, Yang FQ, Li SP, Wang YT, Cui XM. Chemical characteristics for different parts of Panax notoginseng using pressurized liquid extraction and HPLC-ELSD. J Pharmaceut Biomed 2006;41:1591-601.
  4. Liu L, Liu DH, Jin H, Feng GQ, Zhang JY, Wei ML, Zhao ZL. Overview on the mechanisms and control methods of sequential cropping obstacle of Panax notoginseng F.H. Chen. J Mountain Agric Biol 2011;30:70-5 [in Chinese].
  5. Miao ZQ, Li SD, Liu XZ, Chen YJ, Li YH, Wang Y, Guo RJ, Xia ZY, Zhang KQ. The causal microorganisms of Panax notoginseng root rot disease. Sci Agric Sin 2006;39:1371-8 [in Chinese].
  6. Miao CP, Qiao XG, Zheng YK, Chen YW, Xu LH, Guan HL, Zhao LX. First report of Fusarium flocciferum causing root rot of Sanqi (Panax notoginseng) in Yunnan, China. Plant Dis 2015. http://dx.doi.org/10.1094/PDIS-11-14-1168-PDN.
  7. Zhang W, Liao JJ, Zhu GL, Zhang H, Duan XL, Zhu SS, Yang M. The study of inhibitory activity of eight plant volatiles and extracts to Panax notoginseng root rot pathogens. Chinese Agric Sci Bull 2013;29:197-201 [in Chinese].
  8. Moebius-Clune BN, Van Es HM, VanEs OJ, Idowu RR, Schindelbeck JM, Kimetu S, Ngoze J. Long-term soil quality degradation along a cultivation chronosequence in western Kenya. Agr Ecosyst Environ 2011;141:86-99. https://doi.org/10.1016/j.agee.2011.02.018
  9. Singh JS, Pandey VC, Singh DP. Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 2015;140:339-53.
  10. Mohamed HALA, Haggag WM. Biocontrol potential of salinity tolerant mutants of Trichoderma harzianum against Fusarium oxysporum. Braz J Microbiol 2006;37:181-91.
  11. Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM. A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 2007;145:875-89. https://doi.org/10.1104/pp.107.103689
  12. Hohmann P, Jones EE, Hill RA, Stewart A. Understanding Trichoderma in the root system of Pinus radiata: associations between rhizosphere colonisation and growth promotion for commercially seedlings. Fungal Biol UK 2011;115:759-67. https://doi.org/10.1016/j.funbio.2011.05.010
  13. Abada KA. Fungi causing damping-off and root-rot on sugar-beet and their biological control with Trichoderma harzianum. Agric Ecosyst Environ 1994;51:333-7. https://doi.org/10.1016/0167-8809(94)90144-9
  14. Anees M, Tronsmo A, Edel-Hermann V, Hjeljord LG, Heraud C, Steinberg C. Characterization of field isolates of "Trichoderma" antagonistic against 'Rhizoctonia solani'. Fungal Biol UK 2010;114:691-701. https://doi.org/10.1016/j.funbio.2010.05.007
  15. Verma M, Brar SK, Tyagi RD, Surampalli RY, Valero JR. Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 2007;37:1-20. https://doi.org/10.1016/j.bej.2007.05.012
  16. Aochi YO, Farmer WJ. Impact of soil microstructure on the molecular transport dynamics of 1, 2-dichloroethane. Geoderma 2005;127:137-53. https://doi.org/10.1016/j.geoderma.2004.11.024
  17. Dennis C, Webster J. Antagonistic properties of species-groups of 'Trichoderma': II. Production of volatile antibiotics. Trans Br Mycol Soc 1971;57:41-8. IN4. https://doi.org/10.1016/S0007-1536(71)80078-5
  18. Effmert U, Kalderas J, Warnke R, Piechulla B. Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 2012;38:665-703. https://doi.org/10.1007/s10886-012-0135-5
  19. Contreras-Cornejo HA, Macias-Rodriguez L, Herrera-Estrella A, Lopez-Bucio J. The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission. Plant Soil 2014;379:261-74. https://doi.org/10.1007/s11104-014-2069-x
  20. Yang Z, Yu Z, Lei L, Xia Z, Shao L, Zhang K, Li G. Nematicidal effect of volatiles produced by Trichoderma sp. J Asia-pac Entomol 2012;15:647-50. https://doi.org/10.1016/j.aspen.2012.08.002
  21. Fiers M, Lognay G, Fauconnier ML, Jijakli MH. Volatile compound-mediated interactions between barley and pathogenic fungi in the soil. PloS One 2013;8:e66805. https://doi.org/10.1371/journal.pone.0066805
  22. Garbeva P, Hordijk C, Gerards S, De Boer W. Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 2014;87:639-49. https://doi.org/10.1111/1574-6941.12252
  23. Zhang F, Yang X, Ran W, Shen Q. Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum T-E5. FEMS Microbiol Lett 2014;359:116-23. https://doi.org/10.1111/1574-6968.12582
  24. Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 2010;81:187-93. https://doi.org/10.1016/j.mimet.2010.03.011
  25. Crutcher FK, Parich A, Schuhmacher R, Mukherjee PK, Zeilinger S, Kenerley CM. A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genet Biol 2013;56:67-77. https://doi.org/10.1016/j.fgb.2013.05.003
  26. Yang HH, Yang SL, Peng KC, Lo CT, Liu SY. Induced proteome of Trichoderma harzianum by Botrytis cinerea. Mycol Res 2009;113:924-32. https://doi.org/10.1016/j.mycres.2009.04.004
  27. Rothrock CS. Take-all of wheat as affected by tillage and wheat soybean doublecropping. Soil Biol Biochem 1987;19:307-11. https://doi.org/10.1016/0038-0717(87)90014-9
  28. Huang X, Chen L, Ran W, Shen Q, Yang X. Trichoderma harzianum strain SQR-T37 and its bio-organic fertilizer could control Rhizoctonia solani damping off disease incucumber seedlings mainly by the mycoparasitism. Appl Microbiol Biot 2011;91:741-55. https://doi.org/10.1007/s00253-011-3259-6
  29. Gao S, Sosnoskie LM, Cabrera JA, Qin R, Hanson BD, Gerik JS, Wang D, Browne GT, Thomas JE. Fumigation efficacy and emission reduction using low-permeability film in orchard soil fumigation. Pest Manag Sci 2015. http://dx.doi.org/10.1002/ps.3993.
  30. Sun YQ, Yang L, Wei ML, Huang TW. Effects of different treatments and GA3 concentration on induction seedling of Panax notoginseng. Spec Wild Econ Anim Plant Res 2013;04:47-9.
  31. Paz Z, Gerson U, Sztejnberg A. Assaying three new fungi against citrus mites in the laboratory, and a field trial. Biocontrol 2007;52:855-62. https://doi.org/10.1007/s10526-006-9060-2
  32. Spiegel Y, Chet I. Evaluation of Trichoderma spp. as a biocontrol agent against soilborne fungi and plant-parasitic nematodes in Israel. Integr Pest Manage Rev 1998;3:169-75. https://doi.org/10.1023/A:1009625831128
  33. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S. Trichoderma-plant-pathogen interactions: advances in genetics of biological control. Indian J Microbiol 2012;52:522-9. https://doi.org/10.1007/s12088-012-0308-5
  34. Viterbo A, Landau U, Kim S, Chernin L, Chet I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 2010;305:42-8. https://doi.org/10.1111/j.1574-6968.2010.01910.x
  35. Morath SU, Hung R, Bennett JW. Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 2012;26:73-83. https://doi.org/10.1016/j.fbr.2012.07.001
  36. Zhang ZL, Wang WQ, Yang JZ, Cui XM. Effects of continuous Panax notoginseng cropping soil on P. notoginseng seed germination and seedling growth. Soils 2010;42:1009-14 [in Chinese].
  37. Turco E, Vizzuso C, Franceschini S, Ragazzi A, Stefanini FM. The in vitro effect of gossypol and its interaction with salts on conidial germination and viability of Fusarium oxysporum sp. vasinfectum isolates. J Appl Microbiol 2007;103:2370-81. https://doi.org/10.1111/j.1365-2672.2007.03503.x
  38. El-Abyad MS, Hindrof H, Rizk MA. Impact of salinity stress on soil-borne fungi of sugarbeet: II. Growth activities in vitro. Plant Soil 1988;110:33-47. https://doi.org/10.1007/BF02143536
  39. Aydin MH, Turhan G. The efficacy of Trichoderma species against Rhizoctonia solani in potato and their integration with some fungicides. Anadolu 2013;23:12-31.
  40. Gilardi G, Demarchi S, Gullino ML, Garibaldi A. Nursery treatments with non-conventional products against crown and root rot, caused by Phytophthora capsici, on zucchini. Phytoparasitica 2015. http://dx.doi.org/10.1007/s12600-015-0461-6.
  41. Benhamou N, Chet I. Hyphal interactions between Trichoderma harzianum and Rhizoctonia solani: ultrastructure and gold cytochemistry of the mycoparasitic process. Phytopathology 1993;83:1062-71. https://doi.org/10.1094/Phyto-83-1062
  42. Lopez-Mondejar R, Anton A, Raidl S, Ros M, Pascual JA. Quantification of the biocontrol agent Trichoderma harzianum with real-time TaqMan PCR and its potential extrapolation to the hyphal biomass. Bioresource Technol 2010;101:2888-91. https://doi.org/10.1016/j.biortech.2009.10.019
  43. Minerdi D, Bossi S, Gullino ML, Garibaldi A. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol 2009;11:844-54. https://doi.org/10.1111/j.1462-2920.2008.01805.x
  44. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 2003;100:4927-32. https://doi.org/10.1073/pnas.0730845100
  45. Kishimoto K, Matsui K, Ozawa R, Takabayashi J. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 2007;73:35-7. https://doi.org/10.1007/s10327-006-0314-8
  46. Vinale F, Ghisalberti EL, Sivasithamparam K, Marra R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 2009;48:705-11.
  47. Tseng SC, Liu SY, Yang HH, Lo CT, Peng KC. Proteomic study of biocontrol mechanisms of Trichoderma harzianum ETS 323 in response to Rhizoctonia solani. J Agr Food Chem 2008;56:6914-22. https://doi.org/10.1021/jf703626j
  48. Dugravot S, Grolleau F, Macherel D, Rochetaing A, Hue B, Stankiewicz M, Huignard J, Lapied B. Dimethyl disulfide exerts insecticidal neurotoxicity through mitochondrial dysfunction and activation of insect $K_{ATP}$ channels. J Neurophysiol 2003;90:259-70. https://doi.org/10.1152/jn.01096.2002
  49. Kyung KH, Fleming HP. Antimicrobial activity of sulfur compounds derived from cabbage. J Food Prot 1997;60:67-71. https://doi.org/10.4315/0362-028X-60.1.67
  50. Li Y, Mao L, Yan D, Ma T, Shen J, Guo M, Wang Q, Ouyang C, Cao A. Quantification of Fusarium oxysporum in fumigated soils by a newly developed real-time PCR assay to assess the efficacy of fumigants for Fusarium wilt disease in strawberry plants. Pest Manag Sci 2014;70:1669-75. https://doi.org/10.1002/ps.3700
  51. Gu YQ, Mo MH, Zhou JP, Zou CS, Zhang KQ. Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biol Biochem 2007;39:2567-75. https://doi.org/10.1016/j.soilbio.2007.05.011
  52. Spath M, Insam H, Peintner U, Kelderer M, Kuhnert R, Franke-Whittle IH. Linking soil biotic and abiotic factors to apple replant disease: a greenhouse approach. J Phytopathol 2015;163:287-99. https://doi.org/10.1111/jph.12318
  53. Gamliel A, Austerweil M, Kritzman G. Non-chemical approach to soilborne pest management-organic amendments. Crop Prot 2000;19:847-53. https://doi.org/10.1016/S0261-2194(00)00112-5

Cited by

  1. Belowground communication: impacts of volatile organic compounds (VOCs) from soil fungi on other soil-inhabiting organisms vol.100, pp.20, 2016, https://doi.org/10.1007/s00253-016-7792-1
  2. Antifungal, anti‐oomycete and phytotoxic effects of volatile organic compounds from the endophytic fungus Xylaria sp. strain PB3f3 isolated from Haematoxylon brasiletto vol.120, pp.5, 2016, https://doi.org/10.1111/jam.13101
  3. New and bioactive natural products from an endophyte of Panax notoginseng vol.7, pp.60, 2017, https://doi.org/10.1039/c7ra07060h
  4. Integrated Translatome and Proteome: Approach for Accurate Portraying of Widespread Multifunctional Aspects of Trichoderma vol.8, pp.None, 2016, https://doi.org/10.3389/fmicb.2017.01602
  5. Effects of Essential Oils from Zingiberaceae Plants on Root-Rot Disease of Panax notoginseng vol.23, pp.5, 2016, https://doi.org/10.3390/molecules23051021
  6. 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
  7. New 19-Residue Peptaibols from Trichoderma Clade Viride vol.6, pp.3, 2018, https://doi.org/10.3390/microorganisms6030085
  8. Volatile hydrocarbons from endophytic fungi and their efficacy in fuel production and disease control vol.28, pp.1, 2018, https://doi.org/10.1186/s41938-018-0072-x
  9. Endophytic Fungal Volatile Compounds as Solution for Sustainable Agriculture vol.24, pp.6, 2016, https://doi.org/10.3390/molecules24061065
  10. Isolation, Identification and Enzymatic Activity of Halotolerant and Halophilic Fungi from the Great Sebkha of Oran in Northwestern of Algeria vol.47, pp.2, 2016, https://doi.org/10.1080/12298093.2019.1623979
  11. The transcriptome variations of Panaxnotoginseng roots treated with different forms of nitrogen fertilizers vol.20, pp.suppl9, 2016, https://doi.org/10.1186/s12864-019-6340-7
  12. Purification and Characterization of a Novel Antifungal Flagellin Protein from Endophyte Bacillus methylotrophicus NJ13 against Ilyonectria robusta vol.7, pp.12, 2016, https://doi.org/10.3390/microorganisms7120605
  13. Corn and Soybean Host Root Endophytic Fungi with Toxicity Toward the Soybean Cyst Nematode vol.110, pp.3, 2020, https://doi.org/10.1094/phyto-07-19-0243-r
  14. Development of detached root and leaf assays to evaluate the antagonistic properties of biocontrol agents against Fusarium wilt of banana vol.53, pp.9, 2020, https://doi.org/10.1080/03235408.2020.1761222
  15. Roles of Fungal Volatiles from Perspective of Distinct Lifestyles in Filamentous Fungi vol.36, pp.3, 2016, https://doi.org/10.5423/ppj.rw.02.2020.0025
  16. Trichoderma atroviride as a promising biocontrol agent in seed coating for reducing Fusarium damping‐off on maize vol.129, pp.3, 2016, https://doi.org/10.1111/jam.14641
  17. Plants endophytes: unveiling hidden agenda for bioprospecting toward sustainable agriculture vol.40, pp.8, 2020, https://doi.org/10.1080/07388551.2020.1808584
  18. Trichoderma: a beneficial antifungal agent and insights into its mechanism of biocontrol potential vol.30, pp.1, 2016, https://doi.org/10.1186/s41938-020-00333-x
  19. Screening and Identification of Trichoderma Strains isolated from Natural Habitats in China with Potential Agricultural Applications vol.2021, pp.None, 2016, https://doi.org/10.1155/2021/7913950
  20. Biocontrol of rice sheath blight with microorganisms obtained in rice cultivated soils vol.80, pp.None, 2021, https://doi.org/10.1590/1678-4499.20200356
  21. Mycelial Inhibition of Sclerotinia sclerotiorum by Trichoderma spp. Volatile Organic Compounds in Distinct Stages of Development vol.24, pp.4, 2016, https://doi.org/10.3923/pjbs.2021.527.536
  22. Trichoderma spp. in the management of stresses in plants and rural prosperity vol.74, pp.2, 2016, https://doi.org/10.1007/s42360-021-00373-9
  23. Biocontrol Agents: Toolbox for the Screening of Weapons against Mycotoxigenic Fusarium vol.7, pp.6, 2016, https://doi.org/10.3390/jof7060446
  24. Antagonistic Potential of Native Trichoderma spp. against Phytophthora cinnamomi in the Control of Holm Oak Decline in Dehesas Ecosystems vol.12, pp.7, 2021, https://doi.org/10.3390/f12070945
  25. A Critical Review on Communication Mechanism within Plant-Endophytic Fungi Interactions to Cope with Biotic and Abiotic Stresses vol.7, pp.9, 2021, https://doi.org/10.3390/jof7090719
  26. 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
  27. Microbiomes across root compartments are shaped by inoculation with a fungal biological control agent vol.170, pp.None, 2022, https://doi.org/10.1016/j.apsoil.2021.104230
  28. Antagonistic and plant growth promotion effects of Mucor moelleri, a potential biocontrol agent vol.255, pp.None, 2016, https://doi.org/10.1016/j.micres.2021.126922