Skip to main content
Log in

Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The use of specific mycolytic soil microorganisms to control plant pathogens is an ecological approach to overcome the problems caused by standard chemical methods of plant protection. The ability to produce lytic enzymes is a widely distributed property of rhizosphere-competent fungi and bacteria. Due to the higher activity of Trichoderma spp. lytic enzymes as compared to the same class of enzymes from other microorganisms and plants, effort is being aimed at improving biocontrol agents and plants by introducing Trichoderma genes via genetic manipulations. An overview is presented of the data currently available on lytic enzymes from the mycoparasitic fungus Trichoderma.

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.

Similar content being viewed by others

References

  • Antal Z, Manczinger L, Szakas G, Tengerdy RP & Ferencczy L (2000) Colony growth, in vitro antagonism and secretion of extracellular enzymes in cold-tolerant strains of Trichoderma species. Mycol. Res. 104: 545–549.

    Article  CAS  Google Scholar 

  • Baek JM, Howell CR & Kenerley CM (1999) The role of an extracellular chitinase from T. virens Gv29-8 in the biocontrol of Rhizoctonia solani. Curr. Genet. 35: 41–50.

    Article  PubMed  CAS  Google Scholar 

  • Bolar JP, Norelli JL, Wong KW, Hayes CK, Harman GE & Aldwinckle HS (2000) Expression of endochitinase from T. harzianum in transgenic apple increases resistance to apple scab and reduces vigor. Phytopathology 90: 72–77.

    CAS  PubMed  Google Scholar 

  • Carsolio C, Gutierrez A, Jimenez B, van Montagu M & Herrera-Estrella A (1994) Characterization of ech42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proc. Natl. Acad. Sci. USA 91: 10903–10907.

    Article  PubMed  CAS  Google Scholar 

  • Carsolio C, Benhamou N, Haran S, Cortes C, Gutierrez A, Chet I & Herrera-Estrella A (1999) Role of the T. harzianum endochitinase gene, ech42, in mycoparasitism. Appl. Env. Microbiol. 65: 929–935.

    CAS  Google Scholar 

  • Chernin L & Chet I (2001) Microbial enzymes in biocontrol of plant pathogens and pests. In: Burns R & Dicks R (Eds) Enzymes in the Environment: Activity, Ecology and Applications. pp. 171–226 Marcel Dekker, Inc., New York.

    Google Scholar 

  • Cohen-Kupiec R, Broglie KE, Frisem D, Broglie RM & Chet I (1999) Molecular characterization of a novel ß-1,3-exoglucanase related to mycoparasitism of Trichoderma harzianum. Gene 226: 147–154.

    Article  PubMed  CAS  Google Scholar 

  • Collinge DB, Kragh KM, Mikkelnsen JD, Nielsen KK, Rasmussen U & Vad K (1993) Plant chitinases. Plant J. 3: 31–40.

    Article  PubMed  CAS  Google Scholar 

  • Dana MM, Limon. MC, Mejias R, Mach RL, Benitez T, Pintor-Toro JA & Kubicek JP (2001) Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr. Genet. 38: 335–342.

    Article  Google Scholar 

  • Deane EE, Whipps JM, Lynch JM & Peberdy JF (1998) The purification and characterization of a Trichoderma harzianum exochitinase BBA Protein Struct. Mol. Enzym. 1383: 101–110.

    CAS  Google Scholar 

  • de la Cruz J, Hidalgo-Gallego A, Lora JM, Benitez T, Pintor-Toro JA & Llobell A (1992) Isolation and characterization of three chitinases from Trichoderma harzianum. Eur. J. Biochem. 206: 859–867.

    Article  PubMed  CAS  Google Scholar 

  • de la Cruz J, Pintor-Toro JA, Benitez T, Llobell A & Romero LC (1995) A novel endo ß-1,3-glucanase, BGN13.1, involved in the mycoparasitism of Trichoderma harzianum. J. Bacteriol. 177: 6937–6945.

    PubMed  CAS  Google Scholar 

  • Delgado-Jarana J, Pintor-Toro JA & Benitez T (2000) Overproduction of ß-1,6-glucanase in T. harzianum is controlled by extracellular acidic proteases and pH. Biochim. Biophys. Acta 1481: 289–296.

    PubMed  CAS  Google Scholar 

  • De Marco JL, Lima LHC, valle de Sousa M & Felix CR (2000) A Trichoderma harzianum chitinase destroys the cell wall of the phytopathogen Crinipellis perniciosa, the casual agent of witches' broom disease of cocoa. World J. Microbiol. Biotechnol. 16: 383–386.

    Article  CAS  Google Scholar 

  • Draborg H, Kauppinen S, Dalboge H & Christgau S (1995). Molecular cloning and expression in S. cerevisiae of two exochitinases from T. harzianum. Biochem. Molec. Biol. Int. 36: 781–791.

    PubMed  CAS  Google Scholar 

  • Dunaevesky YE, Gruban TN, Beliakova GA & Belozersky MA (2000) Enzymes secreted by filamentous fungi: regulation and purification of an extracellular protease of Trichoderma harzianum. Biochemistry (Mosc). 65: 723–727.

    Google Scholar 

  • El-Katatny MH, Gudelj M, Robra KH, Elnaghy MA & Gübitz GM (2001) Characterization of a chitinase and an endo-ß-1,3-glucanase from T. harzianum Rifai T-24 involved in control of the phytopathogen Sclerotium rolfsii. Appl. Microbiol. Biot. 56: 137–143.

    Article  CAS  Google Scholar 

  • Flores A, Chet I & Herrera-Estrella A (1997) Improved biocontrol activity of T. harzianum strains by overexpression of the proteinase encoding gene prb1. Curr. Genet. 31: 30–37.

    Article  PubMed  CAS  Google Scholar 

  • Garcia I, Lora JM, De la Cruz J, Benitez T, Llobell A & Pintor-Toro JA (1994) Cloning and characterization of a chitinase (CHIT42) cDNA from the mycoparastic fungus T. harzianum. Curr. Genet. 27: 83–89.

    Article  PubMed  CAS  Google Scholar 

  • Haab D, Hagspiel K, Szakmary K & Kubicek CP (1990) Formation of the extracellular protease from T. reesei QM 9414 involved in cellulose degradation. J. Biotechnol. 16: 187–198.

    Article  CAS  Google Scholar 

  • Haran S, Schickler H, Oppenheim AB & Chet I (1995) New components of the chitinolytic system of Trichoderma harzianum. Mycol. Res. 99: 441–446.

    Article  CAS  Google Scholar 

  • Haran S, Schickler H, Oppenheim AB & Chet I (1996) Differential expression of T. harzianum chitinases during mycoparasitism. Phytopathology 86: 980–985.

    CAS  Google Scholar 

  • Harman GE (2000) Myths and dogmas of biocontrol. Plant Dis. 84: 377–391.

    Google Scholar 

  • Harman GE, Hayes CK, Lorito M, Broadway RM, Di Pietro A, Peterbauer C & Tronsmo A (1993) Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase. Phytopathology 83: 313–318.

    CAS  Google Scholar 

  • Herrera-Estrella A & Chet I (1998) Biocontrol of bacteria and phytopathogenic fungi. In: Altman A (Ed). Agricultural Biotechnology pp 263–282. Marcel Dekker Inc. New York.

    Google Scholar 

  • Hui JPM, Lanthier P, White TC, McHugh SG, Yaguchi M, Roy R & Thibault P (2001) Characterization of cellobiohydrolase I (Cel7A) glycoforms from extracts of Trichoderma reesei using capillary isoelectric focusing and electrospray mass spectrometry. J. Chromatogr. 752: 349–368.

    CAS  Google Scholar 

  • Koga K, Iwamoto Y, Sakamoto H, Hatano K, Sano M & Kato I (1991) Purification and characterization of beta-Nacetylhexosaminidase from Trichoderma harzianum. Agric. Biol. Chem. 55: 2817–2824.

    PubMed  CAS  Google Scholar 

  • Kubicek CP, Mach RL, Peterbauer CK & Lorito M (2001) Trichoderma: From genes to biocontrol. J. Plant Pathol. 83: 11–23.

    CAS  Google Scholar 

  • Kulling C, Mach RL, Lorito M & Kubicek CP (2000) Enzyme diffusion from T. atroviride (=T. harzianum P1) to R. solani is a prerequisite for triggering of Trichoderma ech42 gene expression before mycoparasitic contact. Appl. Environ. Microbiol. 66: 2232–2234.

    Article  Google Scholar 

  • Lieckfeldt E, Cavignac Y, Fekete C & Borner T (2000) Endochitinase gene-based phylogenetic analysis of Trichoderma. Microbiol. Res. 155: 7–15.

    PubMed  CAS  Google Scholar 

  • Limon MC, Pintor-Toro JA & Benitez T (1999) Increased antifungal activity of T. harzianum transformants that overexpress a 33-kDa chitinase. Biol. Control 89: 254–261.

    CAS  Google Scholar 

  • Limon MC, Margolles-Clark E, Benitez T & Penttila M (2001) Addition of substrate-binding domains increases substrate binding capacity and specific activity of a chitinase from Trichoderma harzianum. FEMS Microbiol. Lett. 198: 57–63.

    Article  PubMed  CAS  Google Scholar 

  • Lora JM, de la Cruz J, Benitez T, Llobell A & Pintor-Toro A (1995) Molecular characterization and heterologous expression of an endo-ß-1,6-glucanase from the mycoparasitic fungus T. harzianum. Mol. Gen. Genet. 28: 478–483.

    Google Scholar 

  • Lorito M, Harmann GE, Hayes CK, Brodway RM, Woo SL & Di Pietro A (1993) Chitinolitic enzymes produced by T. harzianum. Antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 83: 302–307.

    CAS  Google Scholar 

  • Lorito M, Hayes CK, Di Pietro A, Woo SL & Harman GE (1994) Purification, characterization and synergistic activity of a glucan 1,3-ß-glucosidase and an N-acetylglucosaminidase from T. harzianum. Phytopathology 84: 398–405.

    CAS  Google Scholar 

  • Lorito M, Woo SL, Fernandez IG, Colucci G, Harman GE, Pintor-Toro JA, Filippone E, Muccifora S, Lawrence CB, Zoina A, Tuzun S & Scala F (1998) Genes from mycoparasytic fungi as a source for improving plant resistance to fungal pathogens. Proc. Natl. Acad. Sci. USA 95: 7860–7865.

    Article  PubMed  CAS  Google Scholar 

  • Mach RL, Peterbauer CK, Payer K, Jaksits S, Woo SL, Zeilinger S, Kullnig CM, Lorito M & Kubicek CP (1999) Expression of two major chitinase genes of T. atroviride (T. harzianum P1) is triggered by different regulatory signals. Appl. Environ. Microbiol. 65: 1858–1863.

    PubMed  CAS  Google Scholar 

  • Metcalf DA & Wilson CR (2001). The process of antagonism of Sclerotium cepivorum in white rot affected onion roots by T. koningii. Plant Pathol. 50: 249–257.

    Article  CAS  Google Scholar 

  • Migheli Q, Gonzales-Candelas L, Dealessi L, Camponogara A & Ramon-Vidal D (1998) Transformants of T. longibrachiatum overexpressing the ß-1,4 endoglucanase gene egl1 show enhanced biocontrol of Pythium ultimum on cucumber. Phytopathology 88: 673–677.

    CAS  PubMed  Google Scholar 

  • Mischke S (1996). Evaluation of chromogenic substrates for measurement of protease production by biocontrol strains of Trichoderma. Microbios. 87: 175–183.

    PubMed  CAS  Google Scholar 

  • Mora A & Earle ED (2001) Combination of T. harzianum endochitinase and a membrane-affecting fungicide on control of Alternaria leaf spot in trasgenic broccoli plants. Appl.Microbiol. Biotechnol. 55: 306–310.

    Article  PubMed  CAS  Google Scholar 

  • Park KS & Kloepper JW (2000) Activation of PR1a promoter by rhizobacteria that induce systemic resistance in tobacco against Pseudomonas syringae pv. tabaci. Biol. Control 18: 2–9.

    Article  CAS  Google Scholar 

  • Perrakis A, Wilson KS, Chet I, Oppenheim AB & Vorgias CE (1993) Phylogenetic relationships of chitinases. In: Muzzarelli RAA (Ed) Chitin Enzymology pp 217–232. Atec, Italy.

    Google Scholar 

  • Peterbauer CK, Lorito M, Hayes CK, Harman GE & Kubicek CP (1996) Molecular cloning and expression of the nag1 gene (N-acetyl-beta-D-glucosaminidase-encoding gene) from Trichoderma harzianum P1. Curr. Genet. 30: 325–331.

    Article  PubMed  CAS  Google Scholar 

  • Ramot O, Cohen-Kupiec R & Chet I (2000). Regulation of ß-1,3-glucanase by carbon starvation in the mycoparasite T. harzianum. Mycol. Res. 104: 415–420.

    Article  CAS  Google Scholar 

  • Rey M, Delgado-Jarana J & Benitez T (2001) Improved antifungal activity of a mutant of Trichoderma harzianum CECT 2413 which produces more extracellular proteins. Appl. Microbiol. Biotechnol. 55: 604–608.

    Article  PubMed  CAS  Google Scholar 

  • Sahai AS & Manocha MS (1993) Chitinases of fungi and plants: their involvment in morphogenesis and host-parasite interaction. FEMS Microbiol. Rev. 11: 317–338.

    Article  CAS  Google Scholar 

  • Thrane C, Jensen DF & Tromso A (2000) Substrate colonization, strain competition, enzyme production in vitro, and biocontrol of Pythium ultimum by Trichoderma spp. isolates P1 and T3. Eur. J. Plant Pathol. 106: 215–225.

    Article  CAS  Google Scholar 

  • Ulhoa CJ & Peberdy JF (1991) Purification and characterization of an extracellular chitobiase from T. harzianum. Curr. Microbiol. 23: 285–289.

    Article  CAS  Google Scholar 

  • van Loon LC, Bakker PAHM & Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Ann. Rev. Phytopathol. 36: 453–483.

    Article  CAS  Google Scholar 

  • Viterbo A, Haran S, Friesem D, Ramot O & Chet I (2001) Antifungal activity of a novel endochitinase gene (chit36) from T. harzianum Rifai TM. FEMS Microbiol. Lett. 200: 169–174.

    Article  PubMed  CAS  Google Scholar 

  • Woo SL, Donzelli B, Scala F, Mach R, Harman GE, Kubicek CP, del Sorbo G & Lorito M (1999) Disruption of the ech42 (endochitinase-encoding) gene affects biocontrol activity in T. harzianum P1. Mol. Plant Microbe In. 12: 419–429.

    CAS  Google Scholar 

  • Yedidia I, Benhamou N, Kapulnik Y & Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite T. harzianum strain T-203. Plant Physiol. Biochem. 38: 863–873.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ada Viterbo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Viterbo, A., Ramot, O., Chernin, L. et al. Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens. Antonie Van Leeuwenhoek 81, 549–556 (2002). https://doi.org/10.1023/A:1020553421740

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020553421740

Navigation