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Abstract
A transcriptomic database was constructed to study the biocontrol mechanisms of Trichoderma harzianum ACCC30371 using high quality UniGenes following growth in eight culture media [(1/2PD, minimal medium MM (containing dextrose 10 g L−1), C starvation medium (derived from MM without dextrose), N starvation medium (derived from MM without ammonium sulphate), and four kinds of phytopathogenic fungi cell wall media]. A 4 Gbp transcriptome was generated and 96.7% of the database had a sequencing error rate less than 1%. A total of 25,013 UniGene sequences were obtained with a mean length of 1135 nt. There were 2571 sequences longer than 3000 nt. The National Center for Biotechnology Information Accession number of this transcriptome is SRR8382572. There were 16,360 Unigenes annotated to the Nr protein database, 9875 to the SwissProt database, 10,266 to the KEGG database, 7164 to the COG database, and 1508 to the GO database along with their protein functional annotations. There were 16,723 functional genes identified. We identified 402 bio-control genes, including 14 related to competition, 311 to mycoparasitism, 76 to antibiosis, and one related to eliciting a plant response. This shows that T. harzianum ACCC30371 has integrated biocontrol mechanisms, and of these mechanisms, mycoparasitism is the most prevalent. Antibiosis and induced systemic resistance also play important roles. These results provide a foundation for further research into the biocontrol mechanisms of Trichoderma, as well as the development and utilization of biological fungicides.
Keywords
Biocontrol
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Transcriptome
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Trichoderma harzianum
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Biocontrol genes
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Ruiting Guo, Zhiying Wang, Chang Zhou, Zhihua Liu, Ping Zhang, Haijuan Fan.
Transcriptomic analysis reveals biocontrol mechanisms of Trichoderma harzianum ACCC30371 under eight culture conditions.
Journal of Forestry Research, 2019, 31(5): 1863-1873 DOI:10.1007/s11676-019-00912-1
| [1] |
Anees M, Tronsmo A, Edelhermann V, Hjeljord LG, Héraud C, Steinberg C. Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biol-Uk, 2010, 114: 691-701.
|
| [2] |
Askolin S, Penttilä M, Han ABW, Nakarisetälä T. The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol Lett, 2010, 253: 281-288.
|
| [3] |
Atanasova L, Le CS, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, Druzhinina IS. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genom, 2013, 14: 121-136.
|
| [4] |
Barak R, Elad Y, Mirelman D, Chet I. Lectins: a possible basis for specific recognition in the interaction of Trichoderma and Sclerotium rolfsii. Phytopathology, 1985, 75: 458-462.
|
| [5] |
Baranski RAEV, Nothnagel TH. Chitinase CHIT36 from Trichoderma harzianum enhances resistance of transgenic carrot to fungal pathogens. J Phytopathol, 2010, 156: 513-521.
|
| [6] |
Benítez T, Rincón A, Limón M, Codón A. Biocontrol mechanisms of Trichoderma strains. Int Microbiol, 2004, 7: 249-260.
|
| [7] |
Carpenter M, Stewart A, Ridgway H. Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiol Lett, 2010, 251: 105-112.
|
| [8] |
Carrero-Carrón I, Trapero-Casas JL, Olivares-García C, Monte E, Hermosa R, Jiménez-Díaz RM. Trichoderma asperellum is effective for biocontrol of Verticillium wilt in olive caused by the defoliating pathotype of Verticillium dahliae. Crop Prot, 2016, 88: 45-52.
|
| [9] |
De JR, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, Van DKS, Shibuya N, Joosten MH, Thomma BP. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science, 2010, 329: 953-965.
|
| [10] |
Deng JJ, Huang WQ, Li ZW, Lu DL, Zhang Y, Luo XC. Biocontrol activity of recombinant aspartic protease from Trichoderma harzianum against pathogenic fungi. Enzyme Microb Technol, 2018, 112: 35-42.
|
| [11] |
Djonović S, Pozo M, Dangott L, Howell C, Kenerley C. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe in, 2006, 19: 838-853.
|
| [12] |
Dong ZY, Wang ZZ. Isolation and characterization of an exopolygalacturonase from Fusarium oxysporum f.sp. cubense race 1 and race 4. BMC Biochem, 2011, 12: 51-60.
|
| [13] |
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol, 2011, 9: 749-759.
|
| [14] |
Elad Y, Barak R, Chet I. Possible role of lectins in mycoparasitism. J Bacteriol, 1983, 154: 1431-1435.
|
| [15] |
Gómezrodríguez EY, Urestirivera EE, Patrónsoberano OA, Islasosuna MA, Floresmartínez A, Riegoruiz L, Rosalessaavedra MT, Casasflores S. Histone acetyltransferase TGF-1 regulates Trichoderma atroviride secondary metabolism and mycoparasitism. PLoS One, 2018, 13: e193872.
|
| [16] |
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol, 2004, 2: 43-56.
|
| [17] |
Hermosa R, Viterbo A, Chet I, Monte E. Plant-beneficial effects of Trichoderma and of its genes. Microbiology-SGM, 2012, 158: 17-25.
|
| [18] |
Ji SD, Wang ZY, Fan HJ, Zhang RS, Yu ZY, Wang JJ, Liu ZH. Heterologous expression of the Hsp24 from Trichoderma asperellum improves antifungal ability of Populus transformant Pdpap-Hsp24 s to Cytospora chrysosperma and Alternaria alternata. J Plant Res, 2016, 129: 921-933.
|
| [19] |
Kumar P, Kumar C. Molecular and enzymatic approach to study Trichoderma harzianum—induced disease resistance in Brassica juncea against Albugo candida. J Plant Dis Protect, 2017, 125: 1-9.
|
| [20] |
Liu PG, Yang Q. Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach. Res Microbiol, 2005, 156: 416-423.
|
| [21] |
Liu Z, Yang XX, Sun D, Song J, Chen G, Juba O, Yang Q. Expressed sequence tags-based identification of genes in a biocontrol strain Trichoderma asperellum. Mol Biol Rep, 2010, 37: 3673-3681.
|
| [22] |
Lorito M, Woo S, Harman G, Monte E. Translational research on Trichoderma: from ‘omics to the field. Annu Rev Phytopathol, 2010, 48: 395-418.
|
| [23] |
Mehrabi-Koushki M, Mahdikhani-Moghaddam E. Differential display of abundantly expressed genes of Trichoderma harzianum during colonization of tomato-germinating seeds and roots. Curr Microbiol, 2012, 65: 524-533.
|
| [24] |
Monteiro VN, Silva RDN, Steindorff AS, Costa FT, Noronha EF, Ricart CAO, Sousa MVD, Vainstein MH, Ulhoa CJ. New Insights in Trichoderma harzianum antagonism of fungal plant pathogens by secreted protein analysis. Curr Microbiol, 2010, 61: 298-305.
|
| [25] |
Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutierrez S, Lorito M, Monte E. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum-plant beneficial interaction. Mol Plant Microbe Interact, 2009, 22: 1021-1031.
|
| [26] |
Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods, 2008, 7: 621-628.
|
| [27] |
Mukherjee M, Horwitz BA, Sherkhane PD, Hadar R, Mukherjee PK. A secondary metabolite biosynthesis cluster in Trichoderma virens: evidence from analysis of genes under expressed in a mutant defective in morphogenesis and antibiotic production. Curr Genet, 2006, 50: 193-202.
|
| [28] |
Nicole M. Salicylic acid and ethylene pathways are differentially activated in Melon Cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol, 2001, 127: 334-344.
|
| [29] |
Reithner B, Ibarra-Laclette E, Mach R, Herrera-Estrella A. Identification of mycoparasitism-related genes in Trichoderma atroviride. Appl Environ Microbiol, 2011, 77: 4361-4370.
|
| [30] |
Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A. Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J, 2010, 32: 1049-1055.
|
| [31] |
Rubio M, Domínguez S, Monte E, Hermosa R. Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology-SGM, 2012, 158: 119-128.
|
| [32] |
Samolski I, Luis AD, Vizcaíno JA, Monte E, Suárez MB. Gene expression analysis of the biocontrol fungus Trichoderma harzianum in the presence of tomato plants, chitin, or glucose using a high-density oligonucleotide microarray. BMC Microbiol, 2009, 9: 217-231.
|
| [33] |
Sánchez-Arreguín A, Pérez-Martínez A, Herrera-Estrella A. Proteomic analysis of Trichoderma atroviride reveals independent roles for transcription factors BLR-1 and BLR-2 in light and darkness. Eukaryot Cell, 2012, 11: 30-41.
|
| [34] |
Schenk P, Carvalhais L, Kazan K. Unraveling plant-microbe interactions: can multi-species transcriptomics help?. Trends Biotechnol, 2012, 30: 177-184.
|
| [35] |
Seidl V, Song L, Lindquist E, Gruber S, Koptchinskiy A, Zeilinger S, Schmoll M, Martínez P, Sun J, Grigoriev I. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genom, 2009, 10: 567-580.
|
| [36] |
Seidlseiboth V, Gruber S, Sezerman U, Schwecke T, Albayrak A, Neuhof T, Von DH, Baker SE, Kubicek CP. Novel hydrophobins from Trichoderma define a new hydrophobin subclass: protein properties, evolution, regulation and processing. J Mol Evol, 2011, 72: 339-351.
|
| [37] |
Shentu XP, Liu WP, Zhan XH, Xu YP, Xu JF, Yu XP, Zhang CX. Transcriptome sequencing and gene expression analysis of Trichoderma brevicompactum under different culture conditions. PLoS One, 2014, 9: e94203.
|
| [38] |
Shoresh M, Harman GE, Mastouri F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol, 2010, 48: 21-43.
|
| [39] |
Steindorff AS, Silva RDN, Coelho ASG, Nagata T, Noronha EF, Ulhoa CJ. Trichoderma harzianum expressed sequence tags for identification of genes with putative roles in mycoparasitism against Fusarium solani. Biol Control, 2012, 61: 134-140.
|
| [40] |
Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutiérrez S, Monte E, Hermosa R. Overexpression of the trichodiene synthase gene increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet Biol, 2011, 48: 285-296.
|
| [41] |
Tondje PR, Roberts DP, Bon MC, Widmer T, Samuels GJ, Ismaiel A, Begoude AD, Tchana T, Nyembtshomb E, Ndoumbenkeng M. Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol Control, 2007, 43: 202-212.
|
| [42] |
Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD. Trichoderma: a potential bioremediator for environmental cleanup. Clean Technol Environ Policy, 2013, 15: 541-550.
|
| [43] |
Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol, 2008, 72: 80-86.
|
| [44] |
Viterbo A, Chet I. TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol, 2006, 7: 249-258.
|
| [45] |
Vizcaíno JA, González FJ, Suárez MB, Redondo J, Heinrich J, DelgadoJarana J, Hermosa R, Gutiérrez S, Monte E, Llobell A. Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. BMC Genom, 2006, 7: 193-207.
|
| [46] |
Vizcaíno JA, Redondo J, Suárez MB, Cardoza RE, Hermosa R, González FJ, Rey M, Monte E. Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl Microbiol Biotechnol, 2007, 75: 853-862.
|
| [47] |
Vos CM, De CK, Cammue BP, De CB. The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease. Mol Plant Pathol, 2015, 16: 400-412.
|
| [48] |
Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet, 2009, 10: 57-63.
|
| [49] |
Xing W, Cheng CY, Zhang KJ, Tian Z, Xu J, Yang SQ, Lou QF, Li J, Chen JF. Comparative transcriptomics reveals suppressed expression of genes related to auxin and the cell cycle contributes to the resistance of cucumber against Meloidogyne incognita. BMC Genom, 2018, 19: 583-597.
|