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http://dx.doi.org/10.1016/j.jgr.2018.03.002

Endophytic Trichoderma citrinoviride isolated from mountain-cultivated ginseng (Panax ginseng) has great potential as a biocontrol agent against ginseng pathogens  

Park, Young-Hwan (Department of Biotechnology, Yeungnam University)
Mishra, Ratnesh Chandra (Department of Biotechnology, Yeungnam University)
Yoon, Sunkyung (Department of Biotechnology, Yeungnam University)
Kim, Hoki (Department of Biotechnology, Yeungnam University)
Park, Changho (Enbio)
Seo, Sang-Tae (Division of Forest Insect Pests and Diseases, National Institute of Forest Science)
Bae, Hanhong (Department of Biotechnology, Yeungnam University)
Publication Information
Journal of Ginseng Research / v.43, no.3, 2019 , pp. 408-420 More about this Journal
Abstract
Background: Ginseng (Panax ginseng Meyer) is an invaluable medicinal plant containing various bioactive metabolites (e.g., ginsenosides). Owing to its long cultivation period, ginseng is vulnerable to various biotic constraints. Biological control using endophytes is an important alternative to chemical control. Methods: In this study, endophytic Trichoderma citrinoviride PG87, isolated from mountain-cultivated ginseng, was evaluated for biocontrol activity against six major ginseng pathogens. T. citrinoviride exhibited antagonistic activity with mycoparasitism against all ginseng pathogens, with high endo-1,4-${\beta}$-D-glucanase activity. Results: T. citrinoviride inoculation significantly reduced the disease symptoms caused by Botrytis cinerea and Cylindrocarpon destructans and induced ginsenoside biosynthesis in ginseng plants. T. citrinoviride was formulated as dustable powder and granules. The formulated agents also exhibited significant biocontrol activity and induced ginsenosides production in the controlled environment and mountain area. Conclusion: Our results revealed that T. citrinoviride has great potential as a biological control agent and elicitor of ginsenoside production.
Keywords
Biocontrol agent; Formulation; Fungal endophyte; Ginsenoside; Mountain-cultivated ginseng;
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1 Ernst E. Panax ginseng: an overview of the clinical evidence. J Ginseng Res 2010;34:259-63.   DOI
2 Park JD, Rhee DK, Lee YH. Biological activities and chemistry of saponins from Panax ginseng C. A. Meyer. Phytochem Rev 2005;4:159-75.   DOI
3 Zeilinger S, Omann M. Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul Syst Biol 2007;1:227-34.
4 Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 2006;43:143-8.   DOI
5 Cavalcante RS, Lima HLS, Pinto GAS, Gava CAT, Rodrigues S. Effect of moisture on Trichoderma conidia production on corn and wheat bran by solid state fermentation. Food Bioprocess Technol 2008;1:100-4.   DOI
6 Lin H, Travisano M, Kazlauskas RJ. Experimental evolution of Trichoderma citrinoviride for faster deconstruction of cellulose. PLoS One 2016;11:1-17.
7 Chowdhury EK, Jeon J, Ok Rim S, Park YH, Lee SK, Bae H. Composition, diversity and bioactivity of culturable bacterial endophytes in mountain-cultivated ginseng in Korea. Sci Rep 2017;7:10098. https://doi.org/10.1038/s41598-017-10280-7.   DOI
8 Bae H, Kim SH, Kim MS, Sicher RC, Lary D, Strem MD, Natarajan S, Bailey BA. The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses. Plant Physiol Biochem 2008;46:174-88.   DOI
9 Saikkonen K, Saari S, Helander M. Defensive mutualism between plants and endophytic fungi? Fungal Divers 2010;41:101-13.   DOI
10 Lee O-R, Sathiyaraj G, Kim Y-J, In J-G, Kwon W-S, Kim J-H, Yang DC. Defense genes induced by pathogens and abiotic stresses in Panax ginseng C.A. Meyer. J Ginseng Res 2011;35:1-11.   DOI
11 Soulie MC, Perino C, Piffeteau A, Choquer M, Malfatti P, Cimerman A, Kunz C, Boccara M, Vidal-Cros A. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell Microbiol 2006;8:1310-21.   DOI
12 Martinez-Medina A, Fernandez I, Sanchez-Guzman MJ, Jung SC, Pascual JA, Pozo MJ. Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 2013;4. https://doi.org/10.3389/fpls.2013.00206.
13 Ghosh R, Mishra RC, Choi B, Kwon YS, Bae DW, Park S-C, Jeong M-J, Bae H. Exposure to sound vibrations lead to transcriptomic, proteomic and hormonal changes in Arabidopsis. Sci Rep 2016;6:33370. https://doi.org/10.1038/srep33370.   DOI
14 Kwon KR, Park WP, Kang WM, Jeon EY, Jang JH. Identification and analysis of differentially expressed genes in mountain cultivated ginseng and mountain wild ginseng. J Acupunct Meridian Stud 2011;4:123-8.   DOI
15 Cao R, Liu X, Gao K, Mendgen K, Kang Z, Gao J, Dai Y, Wang X. Mycoparasitism of endophytic fungi isolated from reed on soilborne phytopathogenic fungi and production of cell wall-degrading enzymes in vitro. Curr Microbiol 2009;59:584-92.   DOI
16 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.   DOI
17 Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 1959;31:426-8.   DOI
18 Saroj DB, Dengeti SN, Aher S, Gupta AK. A rapid, one step molecular identification of Trichoderma citrinoviride and Trichoderma reesei. World J Microbiol Biotechnol 2015;31:995-9.   DOI
19 Park SU, Lim HS, Park KC, Park YH, Bae H. Fungal endophytes from three cultivars of Panax ginseng Meyer cultivated in Korea. J Ginseng Res 2012;36:107-13.   DOI
20 Wu Z, Hao Z, Zeng Y, Guo L, Huang L-Q, Wang Y, Chen B-D. Molecular quantification of Cylindrocarpon destructans in the rhizosphere of Panax notoginseng for predicting plant growth response. Microbiol China 2015;42:598-607.
21 Leung KW, Wong AS-T. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5:20. https://doi.org/10.1186/1749-8546-5-20.   DOI
22 Lengeler KB, Davidson RC, D'souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J. Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 2000;64:746-85.   DOI
23 Klimpel A, Gronover CS, Williamson B, Stewart JA, Tudzynski B. The adenylate cyclase (BAC) in Botrytis cinerea is required for full pathogenicity. Mol Plant Pathol 2002;3:439-50.   DOI
24 Schulze Gronover C, Schorn C, Tudzynski B. Identification of Botrytis cinerea genes up-regulated during infection and controlled by the Galpha subunit BCG1 using suppression subtractive hybridization (SSH). Mol Plant Microbe Interact 2004;17:537-46.   DOI
25 McQuilken MP, Gemmell J. Enzyme production by the mycoparasite Verticillium biguttatum against Rhizoctonia solani. Mycopathologia 2004;157:201-5.   DOI
26 Shi J, Liu A, Li X, Chen W. Control of Phytophthora incotianae disease, induction of defense responses and genes expression of papaya frutis treated with Pseudomonas putida MGP1. J Sci Food Agric 2013;93:568-74.   DOI
27 Ali MB, Yu KW, Hahn EJ, Paek KY. Methyl jasmonate and salicylic acid elicitation induces ginsenosides accumulation, enzymatic and non-enzymatic antioxidant in suspension culture Panax ginseng roots in bioreactors. Plant Cell Rep 2006;25:613-20.   DOI
28 Gao Y, Liu Q, Zang P, Li X, Ji Q, He Z, Zhao Y, Yang H, Zhao X, Zhang L. An endophytic bacterium isolated from Panax ginseng C.A. Meyer enhances growth, reduces morbidity, and stimulates ginsenoside biosynthesis. Phytochem Lett 2015;11:132-8.   DOI
29 Garay-Arroyo A, De La Paz Sanchez M, Garcia-Ponce B, Azpeitia E, Alvarez-Buylla ER. Hormone symphony during root growth and development. Dev Dyn 2012;241:1867-85.   DOI
30 Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 2012;28:489-521.   DOI
31 Lian M, Chakrabarty D, Paek K. Effect of plant growth regulators and medium composition on cell growth and saponin production during cell suspension culture of mountaint ginseng (Panax ginseng C.A. Mayer). J Plant Biol 2002;45:201-6.   DOI
32 Ownley BH, Gwinn KD, Vega FE. Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 2010;55:113-28.   DOI
33 Cho KM, Hong SY, Lee SM, Kim YH, Kahng GG, Lim YP, Kim H, Yun HD. Endophytic bacterial communities in ginseng and their antifungal activity against pathogens. Microb Ecol 2007;54:341-51.   DOI
34 Sathiyaraj G, Srinivasan S, Subramanium S, Kim YJ, Kim YJ, Kwon WS, Yang DC. Polygalacturonase inhibiting protein: isolation, developmental regulation and pathogen related expression in Panax ginseng C.A. Meyer. Mol Biol Rep 2010;37:3445-54.   DOI
35 Li HY, Wei DQ, Shen M, Zhou ZP. Endophytes and their role in phytoremediation. Fungal Divers 2012;54:11-8.   DOI
36 Ek-Ramos MJ, Zhou W, Valencia CU, Antwi JB, Kalns LL, Morgan GD, Kerns DL, Sword GA. Spatial and temporal variation in fungal endophyte communities isolated from cultivated cotton (Gossypium hirsutum). PLoS One 2013;8:1-13.
37 Gunatilaka AAL. Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 2006;69:509-26.   DOI
38 Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL, Bailey BA. Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol Plant Microbe Interact 2011;24:336-51.   DOI
39 Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma speciese opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2004;2:43-56.   DOI
40 Kasote DM, Ghosh R, Chung JY, Kim J, Bae I, Bae H, Kasote DM, Ghosh R, Chung JY, Kim J, et al. Multiple reaction monitoring mode based liquid chromatography-mass spectrometry method for simultaneous quantification of brassinolide and other plant hormones involved in abiotic stresses. Int J Anal Chem 2016;2016:1-8.
41 Oh JY, Kim YJ, Jang MG, Joo SC, Kwon WS, Kim SY, Jung SK, Yang DC. Investigation of ginsenosides in different tissues after elicitor treatment in Panax ginseng. J Ginseng Res 2014;38:270-7.   DOI
42 Jang Y, Kim SG, Kim YH. Biocontrol efficacies of Bacillus species against Cylindrocarpon destructans causing ginseng root rot. Plant Pathol J 2011;27:333-41.   DOI
43 Zhang Q, Zhang J, Yang L, Zhang L, Jiang D, Chen W, Li G. Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biol Control 2014;72:98-108.   DOI
44 Alabouvette C, Olivain C, Steinberg C. Biological control of plant diseases: the European situation. Eur J Plant Pathol 2006;114:329-41.   DOI
45 Park YH, Chung JY, Ahn DJ, Kwon TR, Lee SK, Bae I, Yun HK, Bae H. Screening and characterization of endophytic fungi of Panax ginseng Meyer for biocontrol activity against ginseng pathogens. Biol Control 2015;91:71-81.   DOI
46 Schumacher J, Kokkelink L, Huesmann C, Jimenez-Teja D, Collado IG, Barakat R, Tudzynski P, Tudzynski B. The cAMP-dependent signaling pathway and its role in conidial germination, growth, and virulence of the gray mold Botrytis cinerea. Mol Plant Microbe Interact 2008;21:1443-59.   DOI
47 Siewers V, Viaud M, Jimenez-Teja D, Collado IG, Gronover CS, Pradier J-M, Tudzynski B, Tudzynski P. Functional analysis of the cytochrome P450 monooxygenase gene bcbot1 of Botrytis cinerea indicates that botrydial is a strainspecific virulence factor. Mol Plant Microbe Interact 2005;602:602-12.
48 Arguelles JC. Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 2000;174:217-24.   DOI
49 Troian RF, Steindorff AS, Ramada MHS, Arruda W, Ulhoa CJ. Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnol Lett 2014;36:2095-101.   DOI
50 Hu X, Neill S, Cai W, Tang Z. Hydrogen peroxide and jasmonic acid mediate oligogalacturonic acid-induced saponin accumulation in suspension cultured cells of Panax ginseng. Physiol Plant 2003:414-21.
51 Sabaratnam S, Traquair JA. Formulation of a Streptomyces biocontrol agent for the suppression of Rhizoctonia damping-off in tomato transplants. Biol Control 2002;23:245-53.   DOI
52 Perazzolli M, Dagostin S, Ferrari A, Elad Y, Pertot I. Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biol Control 2008;47:228-34.   DOI
53 Shoresh M, Harman GE, Mastouri F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 2010;48:21-43.   DOI
54 Leggett M, Leland J, Kellar K, Epp B. Formulation of microbial biocontrol agents e an industrial perspective. Can J Plant Pathol 2011;33:101-7.   DOI
55 Mauch F, Mauch-Mani B, Boller T. Antifungal hydrolases in pea tissue 1. Plant Physiol 1988;88:936-42.   DOI
56 Pulla RK, Lee OR, In JG, Kim YJ, Senthil K, Yang DC. Expression and functional characterization of pathogenesis-related protein family 10 gene, PgPR10-2, from Panax ginseng C.A. Meyer. Physiol Mol Plant Pathol 2010;74:323-9.   DOI
57 Saboki E, Usha K, Singh B. Pathogenesis related (PR) proteins in plant defense mechanism age-related pathogen resistance. Curr Res Technol Adv 2011:1043-54.
58 Elsharkawy MM, Shimizu M, Takahashi H, Hyakumachi M. The plant growthpromoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae induce systemic resistance against cucumber mosaic virus in cucumber plants. Plant Soil 2012;361:397-409.   DOI
59 Kim YJ, Lee JH, Jung DY, Sathiyaraj G, Shim JS, In JG, Yang DC. Isolation and characterization of pathogenesis-related protein 5 (PgPR5) gene from Panax ginseng. Plant Pathol J 2009;25:400-7.   DOI