Browse > Article
http://dx.doi.org/10.1016/j.jgr.2015.09.006

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)
Publication Information
Journal of Ginseng Research / v.40, no.4, 2016 , pp. 315-324 More about this Journal
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
antagonistic activity; biocontrol agents; mycoparasitism; Panax notoginseng; Trichoderma gamsii;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 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.   DOI
3 Yang HH, Yang SL, Peng KC, Lo CT, Liu SY. Induced proteome of Trichoderma harzianum by Botrytis cinerea. Mycol Res 2009;113:924-32.   DOI
4 Rothrock CS. Take-all of wheat as affected by tillage and wheat soybean doublecropping. Soil Biol Biochem 1987;19:307-11.   DOI
5 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.   DOI
6 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.   DOI
7 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.
8 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.   DOI
9 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.   DOI
10 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].
11 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.   DOI
12 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].
13 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.   DOI
14 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.   DOI
15 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.
16 Mohamed HALA, Haggag WM. Biocontrol potential of salinity tolerant mutants of Trichoderma harzianum against Fusarium oxysporum. Braz J Microbiol 2006;37:181-91.
17 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.   DOI
18 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.   DOI
19 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.   DOI
20 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.   DOI
21 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.   DOI
22 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.   DOI
23 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].
24 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.   DOI
25 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.
26 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.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.   DOI
32 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.
33 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.   DOI
34 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.   DOI
35 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.   DOI
36 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.   DOI
37 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.   DOI
38 Aochi YO, Farmer WJ. Impact of soil microstructure on the molecular transport dynamics of 1, 2-dichloroethane. Geoderma 2005;127:137-53.   DOI
39 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.   DOI
40 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.   DOI
41 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.   DOI
42 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.   DOI
43 Garbeva P, Hordijk C, Gerards S, De Boer W. Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 2014;87:639-49.   DOI
44 Gamliel A, Austerweil M, Kritzman G. Non-chemical approach to soilborne pest management-organic amendments. Crop Prot 2000;19:847-53.   DOI
45 Kyung KH, Fleming HP. Antimicrobial activity of sulfur compounds derived from cabbage. J Food Prot 1997;60:67-71.   DOI
46 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.   DOI
47 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.
48 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.   DOI
49 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.   DOI
50 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.   DOI
51 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].
52 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.
53 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].