Application and Mechanism of Trichoderma in Biological Control of Plant Disease

doi:10.16409/j.cnki.2095-039x.2019.06.025

Abstract

Abstract: Trichoderma spp. are widely studied biological control agents (BCA) and have been used worldwide for plant disease control. The application and control efficiency of Trichoderma in control of plant diseases was reviewed in this paper. The multiple biocontrol mechanisms of Trichoderma against pathogens, including competition, mycoparasitism and antifungal activity, as well as the interaction with plant (plant growth promotion and induced resistance), were summarized. More than 250 Trichoderma-based bio-products have been commercialized and successfully used in different area of the world, exploration of more potential Trichoderma isolates by screening or genetic improvement are still processing. The researches of Trichoderma-based biocontrol and the mechanism have outstanding contributions to the application of biocontrol and the reduction of chemical fungicide use.

Key words: Trichoderma, plant disease, biological control, Trichoderma-based commercial products

CLC Number:

S476

YOU Jiaqi, WU Mingde, LI Guoqing. Application and Mechanism of Trichoderma in Biological Control of Plant Disease[J]. Chinese Journal Of Biological Control, 2019, 35(6): 966-976.

References

[1] Bissett J, Gams W, Jaklitsch W, et al. Accepted Trichoderma names in the year 2015[J]. Ima Fungus, 2015, 6(2):263-295
[2] Kopchinskiy A, Komoń M, Kubicek C P, et al. Tricho blast:A multilocus database for Trichoderma and Hypocrea identifications[J]. Mycological Research, 2005, 109(6):658-660.
[3] Samuels G J. Trichoderma:systematics, the sexual state, and ecology[J]. Phytopathology, 2006, 96(2):195-206.
[4] Ghisalberti E. Anti-infective agents produced by the Hyphomycetes genera Trichoderma and Gliocladium[J]. Current Medicinal Chemistry-Anti-Infective Agents, 2002, 1(4):343-374.
[5] 程丽云, 叶明珍, 张绍升. 食用菌木霉病的病原鉴定[J]. 亚热带农业研究, 2006, 2(1):41-44.
[6] 杨合同. 木霉生物学[M]. 北京:中国大地出版社, 2015.
[7] Harman G E, Howell C R, Viterbo A, et al. Trichoderma species-opportunistic, avirulent plant symbionts[J]. Nature Reviews Microbiology, 2004, 2(1):43-56.
[8] 杨合同. 木霉分类与鉴定[M]. 北京:中国大地出版社, 2009.
[9] Weindling R. Trichoderma lignorum as a parasite of other soil fungi[J]. Phytopathology, 1932, 22(8):837-845.
[10] 屈海泳, 刘连妹, 王雪梅. 木霉菌在生物防治上应用的研究进展[J]. 湖北农业科学, 2009(3):743-746.
[11] Singh R K, Kumar P, Tiwari N N, et al. Role of endochitinase gene and efficacy of Trichoderma against Colletotrichum falcatum Went. causing red rot disease in sugarcane[J]. Sugar Tech, 2014, 16(2):180-188.
[12] de Los Santos-Villalobos S, Guzmán-Ortiz D A, Gómez-Lim M A, et al. Potential use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a biological control agent against anthracnose in mango (Mangifera indica L.)[J]. Biological Control, 2013, 64(1):37-44.
[13] Marzano M, Gallo A, Altomare C. Improvement of biocontrol efficacy of Trichoderma harzianum vs. Fusarium oxysporum f. sp. lycopersici through UV-induced tolerance to fusaric acid[J]. Biological Control, 2013, 67(3):397-408.
[14] Chowdappa P, Mohan K S P, Jyothi L M, et al. Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3[J]. Biological Control, 2013, 65(1):109-117.
[15] Fontenelle A D B, Guzzo S D, Lucon C M M, et al. Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp.[J]. Crop Protection, 2011, 30(11):1492-1500.
[16] Geraldine A M, Lopes F A C, Carvalho D D C, et al. Cell wall-degrading enzymes and parasitism of sclerotia are key factors on field biocontrol of white mold by Trichoderma spp.[J]. Biological Control, 2013, 67(3):308-316.
[17] Malmierca M G, Barua J, Mccormick S P, et al. Novel aspinolide production by Trichoderma arundinaceum with a potential role in Botrytis cinerea antagonistic activity and plant defense priming[J]. Environmental Microbiology, 2015, 17(4):1103-1118.
[18] Contreras-Cornejo H A, Macías-Rodríguez L, Herrera-Estrella A, et al. The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission[J]. Plant and Soil, 2014, 379(1-2):261-274.
[19] Vos C M, de-Cremer K, Cammue B P, et al. The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease[J]. Molecular Plant Pathology, 2014, 16(4):400-412.
[20] Yedidia I, Shoresh M, Kerem Z, et al. Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins[J]. Applied and Environmental Microbiology, 2003, 69(12):7343-7353.
[21] Adb F, Guzzo S D, Cmm L, et al. Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp.[J]. Crop Protection, 2011, 30(11):1492-1500.
[22] Zhang S, Gan Y, Xu B, et al. The parasitic and lethal effects of Trichoderma longibrachiatum against Heterodera avenae[J]. Biological Control, 2014, 72:1-8.
[23] Adams P B. The potential of mycoparasites for biological control of plant diseases[J]. Annual Review of Phytopathology, 1990, 28(1):59-72.
[24] Harman G, Jin X, Stasz T, et al. Production of conidial biomass of Trichoderma harzianum for biological control[J]. Biological Control, 1991, 1(1):23-28.
[25] Abd-El-Motty T, Shatla M. Biological control of white rot disease of onion (Sclerotium cepivorum) by Trichoderma harzianum[J]. Journal of Phytopathology, 1981, 100(1):29-35.
[26] Inbar J, Menendez A, Chet I. Hyphal interaction between Trichoderma harzianum and Sclerotinia sclerotiorum and its role in biological control[J]. Soil Biology and Biochemistry, 1996, 28(6):757-763.
[27] Rojo F G, Reynoso M M, Ferez M, et al. Biological control by Trichoderma species of Fusarium solani causing peanut brown root rot under field conditions[J]. Crop Protection, 2007, 26(4):549-555.
[28] 徐同, 钟静萍, 李德葆. 木霉对土传病原真菌的拮抗作用[J]. 植物病理学报, 1993, 23(1):65-69.
[29] 李海云, 宋晓妍, 张秀省, 等. 拟康宁木霉SMF2防治大白菜软腐病机理研究[J]. 园艺学报, 2012, 7:1373-1379.
[30] 张婷, 朱洁伟, 武向文, 等. 拮抗木霉菌对玉米弯孢叶斑病的诱导抗性作用[J]. 上海交通大学学报(农业科学版), 2011, 4:38-41, 60.
[31] 朱廷恒, 邢小平, 孙顺娣. 木霉T_(97)菌株对几种植物病原真菌的拮抗作用机制和温室防治试验[J]. 植物保护学报, 2004, 31(2):139-144.
[32] Harman G E. Trichoderma not just for biocontrol anymore[J]. Phytoparasitica, 2011, 39(2):103-108.
[33] Lopes F A, Steindorff A S, Geraldine A M, et al. Biochemical and metabolic profiles of Trichoderma strains isolated from common bean crops in the Brazilian Cerrado, and potential antagonism against Sclerotinia sclerotiorum[J]. Fungal Biology, 2012, 116(7):815-824.
[34] Verma M, Brar S K, Tyagi R D, et al. Antagonistic fungi, Trichoderma spp.:panoply of biological control[J]. Biochemical Engineering Journal, 2007, 37(1):1-20.
[35] 孙虎, 杨丽荣, 全鑫, 等. 木霉生防机制及应用的研究进展[J]. 中国农学通报, 2011, 27(3):242-246.
[36] Benítez T, Rincón A M, Limón M C, et al. Biocontrol mechanisms of Trichoderma strains[J]. International Microbiology, 2004, 7(4):249-260.
[37] Chet I, Inbar J. Biological control of fungal pathogens[J]. Applied Biochemistry and Biotechnology, 1994, 48(1):37-43.
[38] 杨萍, 杨谦. 棘孢木霉丝裂原活化蛋白激酶基因task1的克隆及序列分析[J]. 菌物研究, 2012, 4:228-230.
[39] 陈捷. 木霉菌生物学与应用研究-回顾与展望[J]. 菌物学报, 2014, 33(6):1129-1135.
[40] 陈捷. 木霉菌诱导植物抗病性研究新进展[J]. 中国生物防治学报, 2015, 31(5):733-741.
[41] Gruber S G, Seidl-Seiboth V. Self versus non-self:Fungal cell wall degradation in Trichoderma[J]. Microbiology, 2012, 158(1):26-34.
[42] 刘士旺. 生防绿色木霉工程菌的构建及其诱导植物抗病性研究[D]. 杭州:浙江大学, 2003.
[43] Kubicek C P, Herrera-Estrella A, Seidl-Seiboth V, et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma[J]. Genome Biology, 2011, 12(4):40.
[44] 叶小波, 曾千春, 蒋细良. 木霉菌重寄生过程中的酶学研究进展[J]. 中国生物防治, 2009, 25(3):276-280.
[45] Mukherjee M, Mukherjee P K, Horwitz B A, et al. Trichoderma-plant-pathogen interactions:advances in genetics of biological control[J]. Indian Journal of Microbiology, 2012, 52(4):522-529.
[46] Seidl V, Song L, Lindquist E, et al. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey[J]. BMC Genomics, 2009, 10:567.
[47] Gupta V, Tewari S, Bajpai A. Ultrastructure of mycoparasitism of Trichoderma, Gliocladium and Laetisaria species on Botryodiplodia theobromae[J]. Journal of Phytopathology, 1999, 147(1):19-24.
[48] Card S D, Walter M, Jaspers M V, et al. Targeted selection of antagonistic microorganisms for control of Botrytis cinerea of strawberry in New Zealand[J]. Australasian Plant Pathology, 2009, 38(2):183-192.
[49] Atanasova L, Le Crom S, Gruber S, et al. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism[J]. BMC Genomics, 2013, 14:121.
[50] Dos-Reis-Almeida F B, Cerqueira F M, Do Nascimento-Silva R, et al. Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani:evaluation of coiling and hydrolytic enzyme production[J]. Biotechnology Letters, 2007, 29(8):1189-1193.
[51] Reino J L, Guerrero R F, Hernández-Galán R, et al. Secondary metabolites from species of the biocontrol agent Trichoderma[J]. Phytochemistry Reviews, 2007, 7(1):89-123.
[52] Mukherjee P K, Horwitz B A, Kenerley C M. Secondary metabolism in Trichoderma——a genomic perspective[J]. Microbiology, 2012, 158(Pt 1):35-45.
[53] 李纪顺, 陈凯, 杨合同, 等. 木霉抗生性代谢产物研究进展[J]. 农药, 2010, 10:713-716.
[54] 陈凯, 杨合同, 李纪顺, 等. 绿色木霉菌LTR-2孢子提取物的抑菌活性及化学成分分析[J]. 微生物学通报, 2007, 34(3):455-458.
[55] Anitha R, Murugesan K. Production of gliotoxin on natural substrates by Trichoderma virens[J]. Journal of Basic Microbiology, 2005, 45(1):12-19.
[56] Mukherjee P K, Horwitz B A, Herrera-Estrella A, et al. Trichoderma research in the genome era[J]. Annual Review of Phytopathology, 2013(1):105-129.
[57] Vinale F, Flematti G, Sivasithamparam K, et al. Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum[J]. Journal of Natural Products, 2009, 72(11):2032-2035.
[58] Vinale F, Ghisalberti E L, Sivasithamparam K, et al. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens[J]. Letters in Applied Microbiology, 2009, 48(6):705-711.
[59] Liu S Y, Lo C T, Shibu M A, et al. Study on the anthraquinones separated from the cultivation of Trichoderma harzianum strain Th-R16 and their biological activity[J]. Journal of Agricultural and Food Chemistry, 2009, 57(16):7288-7292.
[60] Malmierca M G, Cardoza R E, Alexander N J, et al. Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes[J]. Applied and Environmental Microbiology, 2012, 78(14):4856-4868.
[61] Vinale F, Girona I A, Nigro M, et al. Cerinolactone, a hydroxy-lactone derivative from Trichoderma cerinum[J]. Journal of Natural Products, 2012, 75(1):103-106.
[62] Chugh J K, Wallace B A. Peptaibols:Models for ion channels[J]. Biochemical Society Transactions, 2001, 29(4):565-570.
[63] Collins R P, Halim A F. Characterization of the Major Aroma Constituent of the Fungus Trichoderma viride (Pers.)[J]. Journal Of Agricultural And Food Chemistry, 1972, 20(2):437-438.
[64] Claydon N, Allan M, Hanson J R, et al. Antifungal alkyl pyrones of Trichoderma harzianum[J]. Transactions of the British Mycological Society, 1987, 88(4):503-513.
[65] Dunlop R W, Simon A, Sivasithamparam K, et al. An antibiotic from Trichoderma koningii active against soilborne plant pathogens[J]. Journal of Natural Products, 1989, 52(1):67-74.
[66] Garnica V A, Barrera O S, Muñoz P E, et al. The volatile 6-pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ethylene insensitive 2 functioning[J]. New Physiologist, 2016, 209(4):1496-1512.
[67] Kottb M, Gigolashvili T, Großkinsky D K, et al. Trichoderma volatiles effecting Arabidopsis:from inhibition to protection against phytopathogenic fungi[J]. Frontiers in microbiology, 2015, 6:995.
[68] Schirmböck M, Lorito M, Wang Y L, et al. Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi[J]. Applied and Environmental Microbiology, 1994, 60(12):4364-4370.
[69] Lehman R M, Cambardella C A, Stott D E, et al. Understanding and enhancing soil biological health:the solution for reversing soil degradation[J]. Sustainability, 2015, 7(1):988-1027.
[70] Lorito M, Woo S L, Harman G E, et al. Translational research on Trichoderma:from 'omics to the field[J]. Annual Review of Phytopathology, 2010, 48:395-417.
[71] Cunningham J E, Kuiack C. Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaii[J]. Applied and Environmental Microbiology, 1992, 58(5):1451-1458.
[72] Contreras-Cornejo H A, Macias-Rodriguez L, Cortes-Penagos C, et al. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis[J]. Plant Physiology, 2009, 149(3):1579-1592.
[73] Alonso-Ramirez A, Poveda J, Martin I, et al. Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots[J]. Molecular Plant Pathology, 2015, 15(8):823-831.
[74] Bae H, Roberts D P, Lim H S, et al. Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms[J]. Molecular Plant-Microbe Interactions, 2011, 24(3):336-351.
[75] Shoresh M, Harman G E, Mastouri F. Induced systemic resistance and plant responses to fungal biocontrol agents[J]. Annual Review of Phytopathology, 2010, 48:21-43.
[76] Chepsergon J, Mwanburi L, Kassim M K. Mechanism of drought tolerance in plants using Trichoderma spp.[J]. International Journal of Science and Research, 2014, 3:1592-1595.
[77] Singh M, Sharma O. Trichoderma-A savior microbe in the era of climate change[J]. International Journal of Advanced Biotechnology Research, 2012, 2(4):784-786.
[78] Bigirimana J, De Meyer G, Poppe J, et al. Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum[J]. Mededelingen Van De Faculteit Landbouwkundige En Toegepaste Biologische Wetenschappen, Universiteit Gent, 1997, 62:1001-1007.
[79] Harman G E. Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzinum T-22[J]. Plant Disease, 2000, 84(4):377-393.
[80] 赵蕾, 滕安娜. 木霉对植物的促生及诱导抗性研究进展[J]. 植物保护, 2010, 36(1):43-46.
[81] Shoresh M, Harman G E. The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root:a proteomic approach[J]. Plant Physiology, 2008, 147(4):2147-2163.
[82] Viterbo A, Harel M, Horwitz B A, et al. Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance[J]. Applied and Environmental Microbiology, 2005, 71(10):6241-6246.
[83] Hanson L, Howell C. Elicitors of plant defense responses from biocontrol strains of Trichoderma viren[J]. Phytopathology, 2004, 94(2):171-176.
[84] Zamioudis C, Korteland J, van Pelt J A, et al. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses[J]. The Plant Journal, 2015, 84(2):309-322.
[85] Campos M, Jacobs-Wagner C, Strobel S A. Mycofumigation by the volatile organic compound-producing fungus Muscodor albus induces bacterial cell death through DNA damage[J]. Applied and Environmental Microbiology, 2015, 81(3):1147-1156.
[86] Martínez-Medina A, Van Wees S, Pieterse C M. Airborne signals by Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum[J]. Plant, Cell and Environment, 2017, 40(11):2691-2705
[87] 戚玮真. 生防木霉菌对植物的解盐促生作用及其机制的硏究[D]. 济南:山东师范大学, 2012.
[88] 胡琼, 邵菲菲. 木霉对植物促生作用的研究进展[J]. 安徽农业科学, 2010, 38(10):5077-5079.
[89] Moreno C A, Castillo F, Gonzalez A, et al. Biological and molecular characterization of the response of tomato plants treated with Trichoderma koningiopsis[J]. Physiological and Molecular Plant Pathology, 2009, 74(2):111-120.
[90] Altomare C, Norvell W, Björkman T, et al. Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22[J]. Applied and Environmental Microbiology, 1999, 65(7):2926-2933.
[91] Vargas W A, Mandawe J C, Kenerley C M. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants[J]. Plant Physiology, 2009, 151(2):792-808.
[92] Bharti M K, Sharma A K, Pandey A K, et al. Physiological and biochemical basis of growth suppressive and growth promotory effect of Trichoderma strains on tomato plants[J]. National Academy Science Letters, 2012, 35(5):355-359.
[93] Lee S, Hung R, Yap M, et al. Age matters:the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth[J]. Archives of Microbiology, 2015, 197(5):723-727.
[94] Woo S L, Ruocco M, Vinale F, et al. Trichoderma-based products and their widespread use in agriculture[J]. The Open Mycology Journal, 2014, 8(1):71-126.
[95] Elad Y. Biological control of grape grey mould by Trichoderma harzianum[J]. Crop Protection, 1994, 13(1):35-38.
[96] 李爱华, 李耀忠, 宋莉莉. 紫外线诱变康宁木霉提高酶活力的研究[J]. 宁夏大学学报(自然科学版), 2003, 24(4):389-391.
[97] 邝哲师, 潘木水, 李国立. 木霉的空间诱变效应[J]. 核农学报, 2005, 19(3):195-197.
[98] 虞龙, 张宁. 离子注入微生物诱变育种的研究与应用进展[J]. 微生物学杂志, 2005, 25(2):80-83.
[99] 林英, 吕淑霞, 张蓓蓓, 等. 绿色木霉原生质体诱变筛选纤维素酶高产菌株[J]. 生物技术, 2006, 16(2):50-51.
[100] 杨合同, 唐文华, 李纪顺, 等. 绿色木霉LTR-2菌株的紫外线诱变改良[J]. 中国生物防治学报, 2004, 20(3):182-186.
[101] 田连生. 抗药性木霉菌株的选育及其与多菌灵的协同作用[J]. 核农学报, 2008, 22(1):32-35.
[102] 孙君社, 李雪, 董秀芹. 纤维素酶高产菌株的选育及产酶条件的研究[J]. 北京林业大学学报, 2002, 24(2):83-85.
[103] 王景林, 尹清强, 吴东林, 等.高活力纤维素酶菌株康氏木霉B-7的选育与产酶条件的研究[J]. 生物技术, 1996(6):14-17.
[104] 王强强, 窦恺, 陈捷, 等. 拮抗性木霉菌株抗逆性筛选评价标准与方法[J]. 中国生物防治学报, 2019, 35(1):99-111.
[105] Liu R, Chen L, Jiang Y, et al. Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system[J]. Cell Discovery, 2015, 1:15007.