Skip to main content
Log in

Transcriptomic analysis reveals biocontrol mechanisms of Trichoderma harzianum ACCC30371 under eight culture conditions

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anees M, Tronsmo A, Edelhermann V, Hjeljord LG, Héraud C, Steinberg C (2010) Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biol-Uk 114:691–701

    Article  Google Scholar 

  • Askolin S, Penttilä M, Han ABW, Nakarisetälä T (2010) The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diverse functions in fungal development. FEMS Microbiol Lett 253:281–288

    Article  CAS  Google Scholar 

  • Atanasova L, Le CS, Gruber S, Coulpier F, Seidl-Seiboth V, Kubicek CP, Druzhinina IS (2013) Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genom 14:121–136

    Article  CAS  Google Scholar 

  • Barak R, Elad Y, Mirelman D, Chet I (1985) Lectins: a possible basis for specific recognition in the interaction of Trichoderma and Sclerotium rolfsii. Phytopathology 75:458–462

    Article  CAS  Google Scholar 

  • Baranski RAEV, Nothnagel TH (2010) Chitinase CHIT36 from Trichoderma harzianum enhances resistance of transgenic carrot to fungal pathogens. J Phytopathol 156:513–521

    Article  CAS  Google Scholar 

  • Benítez T, Rincón A, Limón M, Codón A (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    PubMed  Google Scholar 

  • Carpenter M, Stewart A, Ridgway H (2010) Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiol Lett 251:105–112

    Article  CAS  Google Scholar 

  • Carrero-Carrón I, Trapero-Casas JL, Olivares-García C, Monte E, Hermosa R, Jiménez-Díaz RM (2016) Trichoderma asperellum is effective for biocontrol of Verticillium wilt in olive caused by the defoliating pathotype of Verticillium dahliae. Crop Prot 88:45–52

    Article  Google Scholar 

  • De JR, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, Van DKS, Shibuya N, Joosten MH, Thomma BP (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–965

    Article  CAS  Google Scholar 

  • Deng JJ, Huang WQ, Li ZW, Lu DL, Zhang Y, Luo XC (2018) Biocontrol activity of recombinant aspartic protease from Trichoderma harzianum against pathogenic fungi. Enzyme Microb Technol 112:35–42

    Article  CAS  PubMed  Google Scholar 

  • Djonović S, Pozo M, Dangott L, Howell C, Kenerley C (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe in 19:838–853

    Article  CAS  Google Scholar 

  • Dong ZY, Wang ZZ (2011) Isolation and characterization of an exopolygalacturonase from Fusarium oxysporum f.sp. cubense race 1 and race 4. BMC Biochem 12:51–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759

    Article  CAS  PubMed  Google Scholar 

  • Elad Y, Barak R, Chet I (1983) Possible role of lectins in mycoparasitism. J Bacteriol 154:1431–1435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómezrodríguez EY, Urestirivera EE, Patrónsoberano OA, Islasosuna MA, Floresmartínez A, Riegoruiz L, Rosalessaavedra MT, Casasflores S (2018) Histone acetyltransferase TGF-1 regulates Trichoderma atroviride secondary metabolism and mycoparasitism. PLoS One 13:e193872

    Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  PubMed  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology-SGM 158:17–25

    Article  CAS  Google Scholar 

  • Ji SD, Wang ZY, Fan HJ, Zhang RS, Yu ZY, Wang JJ, Liu ZH (2016) 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 129:921–933

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Kumar C (2017) Molecular and enzymatic approach to study Trichoderma harzianum—induced disease resistance in Brassica juncea against Albugo candida. J Plant Dis Protect 125:1–9

    Google Scholar 

  • Liu PG, Yang Q (2005) Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach. Res Microbiol 156:416–423

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Yang XX, Sun D, Song J, Chen G, Juba O, Yang Q (2010) Expressed sequence tags-based identification of genes in a biocontrol strain Trichoderma asperellum. Mol Biol Rep 37:3673–3681

    Article  CAS  PubMed  Google Scholar 

  • Lorito M, Woo S, Harman G, Monte E (2010) Translational research on Trichoderma: from ‘omics to the field. Annu Rev Phytopathol 48:395–418

    Article  CAS  PubMed  Google Scholar 

  • Mehrabi-Koushki M, Mahdikhani-Moghaddam E (2012) Differential display of abundantly expressed genes of Trichoderma harzianum during colonization of tomato-germinating seeds and roots. Curr Microbiol 65:524–533

    Article  CAS  PubMed  Google Scholar 

  • Monteiro VN, Silva RDN, Steindorff AS, Costa FT, Noronha EF, Ricart CAO, Sousa MVD, Vainstein MH, Ulhoa CJ (2010) New Insights in Trichoderma harzianum antagonism of fungal plant pathogens by secreted protein analysis. Curr Microbiol 61:298–305

    Article  CAS  PubMed  Google Scholar 

  • Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutierrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum-plant beneficial interaction. Mol Plant Microbe Interact 22:1021–1031

    Article  PubMed  CAS  Google Scholar 

  • Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 7:621–628

    Article  CAS  Google Scholar 

  • Mukherjee M, Horwitz BA, Sherkhane PD, Hadar R, Mukherjee PK (2006) 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 50:193–202

    Article  CAS  PubMed  Google Scholar 

  • Nicole M (2001) Salicylic acid and ethylene pathways are differentially activated in Melon Cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127:334–344

    Article  PubMed  PubMed Central  Google Scholar 

  • Reithner B, Ibarra-Laclette E, Mach R, Herrera-Estrella A (2011) Identification of mycoparasitism-related genes in Trichoderma atroviride. Appl Environ Microbiol 77:4361–4370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2010) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055

    Article  Google Scholar 

  • Rubio M, Domínguez S, Monte E, Hermosa R (2012) Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology-SGM 158:119–128

    Article  CAS  Google Scholar 

  • Samolski I, Luis AD, Vizcaíno JA, Monte E, Suárez MB (2009) 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 9:217–231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sánchez-Arreguín A, Pérez-Martínez A, Herrera-Estrella A (2012) Proteomic analysis of Trichoderma atroviride reveals independent roles for transcription factors BLR-1 and BLR-2 in light and darkness. Eukaryot Cell 11:30–41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schenk P, Carvalhais L, Kazan K (2012) Unraveling plant-microbe interactions: can multi-species transcriptomics help? Trends Biotechnol 30:177–184

    Article  CAS  PubMed  Google Scholar 

  • Seidl V, Song L, Lindquist E, Gruber S, Koptchinskiy A, Zeilinger S, Schmoll M, Martínez P, Sun J, Grigoriev I (2009) Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genom 10:567–580

    Article  CAS  Google Scholar 

  • Seidlseiboth V, Gruber S, Sezerman U, Schwecke T, Albayrak A, Neuhof T, Von DH, Baker SE, Kubicek CP (2011) Novel hydrophobins from Trichoderma define a new hydrophobin subclass: protein properties, evolution, regulation and processing. J Mol Evol 72:339–351

    Article  CAS  Google Scholar 

  • Shentu XP, Liu WP, Zhan XH, Xu YP, Xu JF, Yu XP, Zhang CX (2014) Transcriptome sequencing and gene expression analysis of Trichoderma brevicompactum under different culture conditions. PLoS One 9:e94203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    Article  CAS  PubMed  Google Scholar 

  • Steindorff AS, Silva RDN, Coelho ASG, Nagata T, Noronha EF, Ulhoa CJ (2012) Trichoderma harzianum expressed sequence tags for identification of genes with putative roles in mycoparasitism against Fusarium solani. Biol Control 61:134–140

    Article  CAS  Google Scholar 

  • Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutiérrez S, Monte E, Hermosa R (2011) Overexpression of the trichodiene synthase gene increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet Biol 48:285–296

    Article  CAS  PubMed  Google Scholar 

  • Tondje PR, Roberts DP, Bon MC, Widmer T, Samuels GJ, Ismaiel A, Begoude AD, Tchana T, Nyembtshomb E, Ndoumbenkeng M (2007) Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol Control 43:202–212

    Article  Google Scholar 

  • Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD (2013) Trichoderma: a potential bioremediator for environmental cleanup. Clean Technol Environ Policy 15:541–550

    Article  CAS  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    Article  CAS  Google Scholar 

  • Viterbo A, Chet I (2006) TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7:249–258

    Article  CAS  PubMed  Google Scholar 

  • Vizcaíno JA, González FJ, Suárez MB, Redondo J, Heinrich J, DelgadoJarana J, Hermosa R, Gutiérrez S, Monte E, Llobell A (2006) Generation, annotation and analysis of ESTs from Trichoderma harzianum CECT 2413. BMC Genom 7:193–207

    Article  CAS  Google Scholar 

  • Vizcaíno JA, Redondo J, Suárez MB, Cardoza RE, Hermosa R, González FJ, Rey M, Monte E (2007) Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl Microbiol Biotechnol 75:853–862

    Article  PubMed  CAS  Google Scholar 

  • Vos CM, De CK, Cammue BP, De CB (2015) The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease. Mol Plant Pathol 16:400–412

    Article  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing W, Cheng CY, Zhang KJ, Tian Z, Xu J, Yang SQ, Lou QF, Li J, Chen JF (2018) 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 19:583–597

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Haijuan Fan.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Project funding: The work was supported by the Fundamental Research Funds of the Central University, China (Grant Number 2572017AA03 and Grant Number 2572014BA15).

The online version is available at http://www.springerlink.com

Corresponding editor: Tao Xu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, R., Wang, Z., Zhou, C. et al. Transcriptomic analysis reveals biocontrol mechanisms of Trichoderma harzianum ACCC30371 under eight culture conditions. J. For. Res. 31, 1863–1873 (2020). https://doi.org/10.1007/s11676-019-00912-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-019-00912-1

Keywords

Navigation