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Trichoderma Secondary Metabolites: Their Biochemistry and Possible Role in Disease Management

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Microbial-mediated Induced Systemic Resistance in Plants

Abstract

The extensive use of pesticides affected soil quality, water quality and ecological balance and ultimately damaged the socio-economical scenario. The pesticide resistance is also one of the alarming problems of this century. Biological method of sustainable agriculture is the only way to overcome these problems. The current chapter focuses on the use of Trichoderma as biocontrol agent in present agriculture system and its advantages over traditional pesticides and fertilisers. Trichoderma spp. exhibited a wide range of secondary metabolites (volatile, nonvolatile, diffusable) responsible for the protection of plants from harmful pests, nutrient support, mineral solubilisation and pharmacological activities. Trichoderma showed mycoparasitism, antibiosis and competition mechanisms to combat major agricultural pests. The collective information of secondary metabolism, mechanism of action and applications would be useful to biologists, chemists and agriculturists for integrated pest and disease management.

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References

  • Abdullah F, Nagappan J, Sebran NH (2005) Biomass production of Trichoderma harzianum Rifai in palm oil mill effluents (pome). Int J Biol Biotechnol 2(3):571–575

    Google Scholar 

  • Afify A, Abo-El-Seoud MA, Ibrahim GM et al (2013) Stimulating of biodegradation of oxamyl pesticide by low dose gamma irradiated fungi. J Plant Pathol Microbiol 4:201

    Google Scholar 

  • Ahmad JS, Baker R (1987) Competitive saprophytic ability and cellulolytic activity of rhizosphere-competent mutants of Trichoderma harzianum. Phytopathology 77:358–362

    CAS  Google Scholar 

  • Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. Eur J Plant 114:329–341

    Google Scholar 

  • Almassi F, Ghisalberti EL, Narbey MJ (1991) New antibiotics from strains of Trichoderma harzianum. J Nat Prod 54:396–402

    CAS  Google Scholar 

  • Aloj V, Vinale F, Woo S et al (2009) Use of a Trichoderma spp. Enzyme mixture to increase feed digestibility and degrade mycotoxins. J Plant Pathol 91:45–96

    Google Scholar 

  • Anke H, Kinn J, Bergquist KE (1991) Production of siderophores by strains of the genus Trichoderma. Isolation and characterization of the new lipophilic coprogen derivative, palmitoylcoprogen. Bio Metals 4(3):176–180

    Google Scholar 

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

    CAS  Google Scholar 

  • Asalmol MN, Awasthi J (1990) Role of temperature and pH in antagonism of Aspergillus niger and Trichoderma viride against Fusarium solani. In: Proceedings of the All India Phytopathological Society (West Zone). MPAU, Pune, pp 11–13

    Google Scholar 

  • Augeven-Bour I, Rebuffat S, Auvin C et al (1997) Harzianin HB I, an 11-residue peptaibol from Trichoderma harzianum: isolation, sequence, solution synthesis and membrane activity. J Chem Soc Perkin Trans 1(10):1587–1594

    Google Scholar 

  • Auvin-Guette C, Rebuffat S, Prigent Y et al (1992) Trichogin A IV, an ll-residue lipopeptaibols from Trichoderma longibrachiatum. J Am Chem Soc 114:2170–2174

    CAS  Google Scholar 

  • Auvin-Guette C, Rebuffat S, Viudepot I et al (1993) Structural elucidation of trikoningins KA and KB peptaibols from Trichoderma koningii. J Chem Soc Perkin Trans 1:249–255

    Google Scholar 

  • Ayers WA, Adams PB (1981) Mycoparasitism and its application to biological control of plant diseases. In: Papavizas GC (ed) Biological control in crop production, vol 5, BARC Symposium. Allanheld & Osmun, Totowa, pp 91–103

    Google Scholar 

  • Baker R (1988) Trichoderma spp. as plant growth stimulants. CRC Crit Rev Biotechnol 7:97–106

    Google Scholar 

  • Baker R, Paulitz TC (1996) Theoretical basis for microbial interactions leading to biological control of soilborne plant pathogens. In: Hall R (ed) Principles and practice of managing soilborne plant pathogens. APS Press The American Phytopathological Society, St. Paul, pp 50–79

    Google Scholar 

  • Baldwin JE, Harjinder SB, Chondrogianni J et al (1985) Biosynthesis of 3-(3′-isocyanocyclopent- 2-enylidene) propionic acid by Trichoderma hamatum (Bon.) Bain, aggr. Tetrahedron 41:1931–1938

    CAS  Google Scholar 

  • Baldwin NA., Capper AL, Yarham DL (1991) Evaluation of biological agents for the control of take–all patch (Gaeumannomyces graminis) of fine turf. In: A.B.R.e.a. Beemster (ed) Developments in agricultural and manages-forest ecology. Elsevier Science Publishers, Amsterdam, pp 231–235

    Google Scholar 

  • Barakat FM, Abada KA, Abou-Zeid NM et al (2014) Effect of volatile and non-volatile compounds of Trichoderma spp. on Botrytis fabae the causative agent of faba bean chocolate spot. Am J Life Sci 2(6–2):11–18

    Google Scholar 

  • Barbosa M, Rehm K, Menezes M et al (2001) Antagonism of Trichoderma species on Cladosporium herbarum and their enzymatic characterization. Braz J Microbiol 32:98–104

    CAS  Google Scholar 

  • Bebber DP, Ramotowski MAT, Gurr SJ (2013) Crop pests and pathogens move polewards in a warming world. Nat Clim Chang 3:985–988

    Google Scholar 

  • Bell DK, Wells HD, Markham CR (1982) In vitro antagonism of Trichoderma species against six fungal plant pathogens. Phytopathology 72:379–382

    Google Scholar 

  • Benitez T, Rincon AM, Limon MC et al (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260

    CAS  PubMed  Google Scholar 

  • Bodo B, Rebuff S, El Hajji M (1985) Structure of trichorzianine A IIIc, an antifungal peptide from Trichoderma harzianum. J Am Chem Soc 107:6011–6017

    CAS  Google Scholar 

  • Bonnarme P, Djian A, Latrasse A et al (1997) Production of 6-pentyl-α-pyrone by Trichoderma sp. from vegetable oils. J Biotechnol 56:143–150

    CAS  Google Scholar 

  • Brain PW (1944) Production of Gliotoxin by Trichoderma viride. Nature 154:667–668

    Google Scholar 

  • Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites – strategies to activate silent gene clusters. Fungal Genet Biol 48(1):15–22

    CAS  PubMed  Google Scholar 

  • Brasier CM (1975) Stimulation of sex organ formation in Phytophthora by antagonistic species of Trichoderma I, The effects in vitro. New Physiol 74:183–194

    Google Scholar 

  • Brewer D, Feicht A, Taylor A et al (1982) Ovine ill-thrift in Nova Scotia. 9. Production of experimental quantities of isocyanide metabolites of Trichoderma hamatum. Can J Microbiol 28:1252–1260

    CAS  PubMed  Google Scholar 

  • Brewer D, Mason FG, Taylor A (1987) The production of alamethicins by Trichoderma spp. Can J Microbiol 33:619–625

    CAS  PubMed  Google Scholar 

  • Brian PW, McGowan JC (1945) Viridin: a highly fungistatic substance produced by Trichoderma viride. Nature 156:144–145

    CAS  Google Scholar 

  • Bruce A, Austin WJ, King B (1984) Control of growth of Lentinus lepideus by volatiles from Trichoderma. Trans Br Mycol Soc 82:423–428

    Google Scholar 

  • Bruckner H, Graf H (1983) Paracelsin, a peptide antibiotic containing alpha-aminoisobutyric acid, isolated from Trichoderma reesei Simmons. Part A. Experimentia 39(5):528–530

    CAS  Google Scholar 

  • Bruckner H, Przybylski M (1984) Isolation and structural characterization of polypeptide antibiotics of the peptaibol class by high-performance liquid chromatography with field desorption and fast atom bombardment mass spectrometry. J Chromatogr 296:263–275

    Google Scholar 

  • Bues R, Bussieres P, Dadomo M et al (2004) Assessing the environmental impacts of pesticides used on processing tomato crops. Agr Ecosyst Environ 102:155–162

    CAS  Google Scholar 

  • Caldwell R (1958) Fate of spores of Trichoderma viride Pers. Ex. Ft. introduced in the soil. Nature 181:1144–1145

    Google Scholar 

  • Carsolio C, Gutierrez A, Jimenez B et al (1994) Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proc Natl Acad Sci USA 91(23):10903–10907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo-Cadena J, Tenorio-Vieyra LE, Quintana-Carabia AI et al (2006) Determination of DNA damage in floriculturists exposed to mixtures of pesticides. J Biomed Biotechnol 2:1–12

    Google Scholar 

  • Chantrapromma SS, Jeerapong CC, Phupong W et al (2014) Trichodermaerin: a diterpene lactone from Trichoderma asperellum. Acta Crystallogr Sect E Struct Rep Online 70:o408–o409

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chet I (1987) Trichoderma – application, mode of action, and potential as a biocontrol agent of soil borne pathogenic fungi. In: Chet I (ed) Innovative approaches to plant disease control. Wiley, New York, pp 137–160

    Google Scholar 

  • Chet I, Inbar J, Hadar I (1997) Fungal antagonists and mycoparasites. In: Wicklow DT, Soderstrom B (eds) The mycota IV: environmental and microbial relationships. Springer-Verlag, Berlin, pp p165–p184

    Google Scholar 

  • Chet I, Benhamou N, Haran S (1998) Mycoparasitism and lytic enzymes: Trichoderma and Gliocladium. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol 2, Enzymes, Biological Control and Commercial Applications. Taylor & Francis Ltd, London, pp 153–171

    Google Scholar 

  • Chugh JK, Wallace BA (2001) Peptaibols: models for ion channels. Biochem Soc Trans 29:565–570

    CAS  PubMed  Google Scholar 

  • Claydon N, Allan M, Hanson JR et al (1987) Antifungal alkyl pyrones of Trichoderma harzianum. Trans Br Mycol Soc 88(4):503–513

    CAS  Google Scholar 

  • Claydon N, Hanson JR, Truneh A et al (1991) Harzianolide, a butenolide metabolite from cultures of Trichoderma harzianum. Phytochemistry 30:3802–3803

    CAS  Google Scholar 

  • Coats JH, Meyer CE, Pyke TR (1971) Antibiotic dermadin. US Patent 3627882, 14 Dec 1971

    Google Scholar 

  • Collins RP, Halim AF (1972) Characterization of the major aroma constituent of the fungus Trichoderma viride (Pers.). J Agric Food Chem 20:437–438

    CAS  Google Scholar 

  • Cook RJ (1993) Making greater use of introduced micro-organisms for biological control of plant pathogens. Annu Rev Phytopathol 31:53–80

    CAS  PubMed  Google Scholar 

  • Copping LG, Menn JJ (2000) Biopesticides: a review of their action, applications and efficacy. Pest Manag Sci 56:651–676

    CAS  Google Scholar 

  • Corley DG, Miller-Wideman M, Durley RC (1994) Isolation and structure of harzianum A: a new trichothecene from Trichoderma harzianum. J Nat Prod 57:422–425

    CAS  PubMed  Google Scholar 

  • Cutler HG, Jacyno JM, Phillips RS et al (1991) Cyclonerodiol from a novel source, Trichoderma koningii: plant growth regulatory activity. Agric Biol Chem 55:243–244

    CAS  Google Scholar 

  • Dagenais TR, Keller NP (2009) Pathogenesis of Aspergillus fumigatus in invasive Aspergillosis. Clin Microbiol Rev 22(3):447–465

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daniel J, Filho ER (2007) Peptaibols of Trichoderma. Nat Prod Rep 24:1128–1141

    CAS  PubMed  Google Scholar 

  • Danielson RM, Davey CB (1973) Non nutritional factors affecting the growth of Trichoderma in culture. Soil Biol Biochem 5:495–504

    CAS  Google Scholar 

  • Daoubi M, Pinedo-Rivilla C, Rubio MB et al (2009) Hemisynthesis and absolute configuration of novel 6-pentyl-2H-pyran-2-one derivatives from Trichoderma spp. Tetrahedron 69:4834–4840

    Google Scholar 

  • Darmayasa BG, Putra S, Sujaya IN, Sukrama IDM (2014) The Trichoderma asperillum TKD filtrate potency in reducing contaminants of aflatoxins B1 produced by Aspergillus flavus FNCC 6109 on concentrate feed. Int J Pure Appl Biosci 2(6):279–285

    Google Scholar 

  • Deetae P, Bonnarme P, Spinnler HE et al (2007) Production of volatile aroma compounds by bacterial strains isolated from different surface-ripened French cheeses. App Micro Biotechnol 76:1161–1171

    CAS  Google Scholar 

  • Dekker J, Georgopoulos SG (1982) Fungicide resistance in crop protection. Centre for Agricultural Publishing and Documentation, Wageningen, p 265

    Google Scholar 

  • Delgado-Jarana J, Rincon AM, Ben’otez T (2002) Aspartyl protease from Trichoderma harzianum CECT 2413: cloning and characterization. Microbiology 148:1305–1315

    CAS  PubMed  Google Scholar 

  • Dennis C, Webster J (1971a) Antagonistic properties of species-groups of Trichoderma. I. Production of non-volatile antibiotics. Trans Br Mycol Soc 57:25–39

    CAS  Google Scholar 

  • Dennis C, Webster J (1971b) Antagonistic properties of species-groups of Trichoderma. II. Production of volatile antibiotics. Trans Br Mycol Soc 57:41–48

    CAS  Google Scholar 

  • Di Pietro A, Lorito M, Hayes C et al (1993) Endochitinase from Gliocladium virens. Isolation, characterization, synergistic antifungal activity in combination with gliotoxin. Phytopathology 83:308–313

    Google Scholar 

  • Dickinson JM, Hanson JR, Hitchcock PB et al (1989) Claydon N. Structure and biosynthesis of harzianopyridone, an antifungal metabolite of Trichoderma harzianum. J Chem Soc Perkin Trans 1:1885–1887

    Google Scholar 

  • Dickinson JM, Hanson JR, Truneh A (1995) Metabolites of some biological control agents. Pestic Sci 44:389–393

    CAS  Google Scholar 

  • Dix NJ, Webster J (1995) Fungal ecology. Chapman and Hall, London

    Google Scholar 

  • Doan LT, El-Hajii M, Rebuffat S et al (1986) Fluorescein studies on the interaction of trichorzianine A IIIc with model membranes. Biochim Biophys Acta 858:1–5

    PubMed  Google Scholar 

  • Domsch KH, Gams W, Anderson TH (1980) Compendium of soil fungi. Academic, England, p 865

    Google Scholar 

  • Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A et al (2011) Trichoderma: the genomics of opportunistic success. Nat Microbiol Rev 16:749–759

    Google Scholar 

  • Dubey SC, Tripathi A, Dureja P, Grover A (2011) Characterization of secondary metabolites and enzymes produced by Trichoderma species and their efficacy against plant pathogenic fungi. Indian J Agric Sci 81(5):455–461

    CAS  Google Scholar 

  • Dunlop RW, Simon A, Sivasithamparam K (1989) An antibiotic from Trichoderma koningii active against soilborne plant pathogens. J Nat Prod 52:67–74

    CAS  Google Scholar 

  • Duval D, Cosette P, Rebuffat S (1998) Alamethicin-like behaviour of new 18-residue peptaibols, trichorzins PA. Role of the C-terminal amino-alcohol in the ion channel forming activity. BBA-Biomembr 1369:309–319

    CAS  Google Scholar 

  • Edenborough MS, Herbert RB (1988) Naturally occurring isocyanides. Nat Prod Rep 5:229–245

    CAS  PubMed  Google Scholar 

  • Eisendle M, Oberegger H, Buttinger R et al (2004) Biosynthesis and uptake of siderophores is controlled by the Pac mediated ambient-pH regulatory system in Aspergillus nidulans. Eukaryot Cell 3:561–563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisendle M, Schrettl M, Kragl C et al (2006) The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryot Cell 5:1596–1603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elad Y (1996) Mechanisms involved in the biological control of Botrytis cinerea incited diseases. Eur J Plant Pathol 102:719–732

    Google Scholar 

  • Elad Y, Kapat A (1999) The role of Trichoderma harzianum protease in the biocontrol of Botrytis cinerea. EurJ Plant Pathol 105:177–189

    CAS  Google Scholar 

  • El-Hassan A, Buchennauer H (2009) Action of 6-penthyl-alpha pyrone in controlling seedling blight incited by Fusarium moniliforme and inducing defence responses in maize. J Phytopathol 157:697–707

    Google Scholar 

  • Elke K, Begerow J, Oppermann H et al (1999) Determination of selected microbial volatile organic compounds by diffusive sampling and dual-column capillary GC-FID – a new feasible approach for the detection of an exposure to indoor mould fungi? J Environ Monit 1:445–45210

    CAS  PubMed  Google Scholar 

  • Evidente A, Cabras A, Maddau L et al (2003) Viridepyrone, a new antifungal 6-substituted 2H-pyran-2-one produced by Trichoderma viride. J Agric Food Chem 51:6957–6960

    CAS  PubMed  Google Scholar 

  • Faull JL, Graeme-Cook KA, Pilkington BL (1994) Production of an isonitrile antibiotic by an UV-induced mutant of Trichoderma harzianum. Phytochemistry 36:1273–1276

    CAS  PubMed  Google Scholar 

  • Federal Register (1992) Statement of policy: foods derived from new plant varieties; notice. Part IX, Department of Health and Human Services, Food and Drug Administration 57(104):22984–23005

    Google Scholar 

  • Federici BA (1999) Bacillus thuringiensis in biological control. In: Fisher (ed) Handbook of biological control. Academic press, New York, p 575–593

    Google Scholar 

  • Fedorinchik NS, Tarunina TA, Tyunnikov MG et al (1975) Trichoderma in-4, a new biological preparation for plant disease control. 8th Int Congress Plant Prot 3:67–72

    Google Scholar 

  • Fischer E (1906) Synthese von polypeptiden. Chem Ber 39:2893–2931

    CAS  Google Scholar 

  • Fuji K, Fujita E, Takaishi K et al (1978) New antibiotics, trichopolyns A and B: isolation and biological activity. Experientia 34(2):237–239

    CAS  PubMed  Google Scholar 

  • Fujita T, Wada S, Iida A (1994) Fungal metabolites. XIII. Isolation and structural elucidation of new peptaibols, trichodecenins-I and -II, from Trichoderma viride. Chem Pharm Bull 42:489–494

    CAS  Google Scholar 

  • Fujiwara A, Okuda T, Masuda S et al (1982) Isonitrile antibiotics, a new class of antibiotics with an isonitrile group. I. Fermentation, isolation and characterization of isonitrile antibiotics. Agric Biol Chem 46:1803–1809

    CAS  Google Scholar 

  • Gadgil N, Daginawala HF, Chokrabarti T et al (1995) Enhanced cellulase production by a mutant of Trichoderma reesei. Enzym Microbial Technol 17:942–946

    CAS  Google Scholar 

  • Gajera HP, Bambharolia RP, Patel SV et al (2012) Antagonism of Trichoderma spp. against Macrophomina phaseolina: Evaluation of coiling and cell wall degrading enzymatic activities. J Plant Pathol Microbiol 3:7

    Google Scholar 

  • Gams W, Bissett J (1998) Morphology and identification of Trichoderma. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium. Taylor & Francis, London, pp p3–p31

    Google Scholar 

  • Garcia I, Lora LM, De la Cruz J et al (1994) Cloning and characterization of a chitinase (Chit42) cDNA from the mycoparasitic fungus Trichoderma harzianum. Curr Genet 27(1):83–89

    CAS  PubMed  Google Scholar 

  • Gerhardson B (2002) Biological substitutes for pesticides. Trends Biotechnol 20:338–343

    CAS  PubMed  Google Scholar 

  • Ghisalberti EL (1993) Detection and isolation of bioactive natural products. In: Colegate SM, Molyneux RJ (eds) Bioactive natural products: detection, isolation and structure elucidation. CRC Press, Boca Raton, pp 15–18

    Google Scholar 

  • Ghisalberti EL, Sivasithamparam K (1991) Antifungal antibiotics produced by Trichoderma spp. Soil Biol Biochem 23:1011–1020

    CAS  Google Scholar 

  • Ghisalberti EL, Rowland CY (1993) Antifungal metabolites from Trichoderma harzianum. J Nat Prod 56:1799–1804

    CAS  PubMed  Google Scholar 

  • Ghisalberti EL, Narbey MJ, Dewan MM et al (1990) Variability among strains of Trichoderma harzianum in their ability to reduce take-all and to produce pyrones. Plant Soil 121:287–291

    CAS  Google Scholar 

  • Godtfredsen WO, Vangedak S (1965) Trichodermin, a new sesquiterpene antibiotic. Acta Chem Scand Acta Chem Scand 19(5):1088–1102

    CAS  PubMed  Google Scholar 

  • Goulard C, Hlimi S, Rebuffat S, Bodo B (1995) Trichorzins HA and MA, antibiotic peptides from Trichoderma harzianum. I: Fermentation, isolation and biological properties. J Antibiot 48:1248–1253

    CAS  Google Scholar 

  • Graeme-Cook KA, Faull JL (1991) Effect of ultraviolet induced mutants of Trichoderma harzianum with altered antibiotic production of selected pathogens in vitro. Can J Microbiol 37:659–664

    CAS  PubMed  Google Scholar 

  • Grove JF, Mcloskey JP, Moffatt JS (1996) Viridin, Part V. structure. J Chem Soc C 743–747

    Google Scholar 

  • Hahn S, Zhong XY, Holzgreve W (2002) Single cell PCR in laser capture microscopy. Methods Enzymol 356:295–301

    CAS  PubMed  Google Scholar 

  • Hajji EI, Rebuffat M, Lecommandeur SD et al (1987) Isolation and determination trichorzianines A antifungal peptides from Trichoderma harzianum. Int J Pept Protein Res 29:207–215

    PubMed  Google Scholar 

  • Hajji EL, Rebuffat MS, Le Doan T (1989) Interaction of trichorzianines A and B with model membranes and with amoeba Dictyostelium. Biochim Biophys Acta 978:97–104

    PubMed  Google Scholar 

  • Hamilton D, Ambrus A, Dieterle R et al (2004) Pesticide residues in food – acute dietary exposure. Pest Manag Sci 60(4):311–339

    CAS  PubMed  Google Scholar 

  • Haran S, Schickler H, Oppenheim A et al (1996) Differential expression of Trichoderma harzianum chitinases during mycoparasitism. Phytopathology 86:980–985

    CAS  Google Scholar 

  • Harman GE (2000) Myths and dogmas of biocontrol. Changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84:377–393

    CAS  PubMed  Google Scholar 

  • Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194

    CAS  PubMed  Google Scholar 

  • Harman GE, Bjorkman T (1998) Potential and existing uses of Trichoderma and Gliocladium for plant disease control and plant growth enhancement. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol 2. Taylor & Francis Ltd, London, pp 229–266

    Google Scholar 

  • Harman GE, Kubicek CP (eds) (1998) Trichoderma and Gliocladium, vol 2. Taylor & Francis Ltd., London

    Google Scholar 

  • Harman GE, Howell CR, Viterbo A et al (2004) Trichoderma species–opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    CAS  PubMed  Google Scholar 

  • Harmnan GE, Hayes CK, Lorito M et al (1993) Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase. Phytopathology 83:313–318

    Google Scholar 

  • Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean-Rhizobium-Glomus associations. New Phytol 101:427–440

    CAS  PubMed  Google Scholar 

  • Healy FG, Wach M, Krasnoff SB et al (2000) The txt AB genes of the plant pathogen Streptomyces acidiscabies encode a peptide synthetase required for phytotoxin thaxtomin A production and pathogenicity. Mol Microbiol 38:794–804

    CAS  PubMed  Google Scholar 

  • Healy AR, Vinale F, Lorito M (2015) Total synthesis and biological evaluation of the tetramic acid based natural product harzianic acid and its stereoisomers. Org Lett 17:692–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henis Y (1984) Interactions between Sclerotium rolfsii and Trichoderma spp. Relationship between antagonism and disease control. Soil Biol Biochem 16(4):391–395

    Google Scholar 

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

    Google Scholar 

  • Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657

    CAS  PubMed  Google Scholar 

  • Hill RA, Cutler HG, Parker SR (1995) Trichoderma and metabolites as control agents for microbial plant diseases. PCT Int. Appl. WO 95 20879 Chem Abstr 123:220823

    Google Scholar 

  • Hjeljord L, Tronsomo A (1988) Trichoderma and Gliocladium in biological control: an overview. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium. Taylor & Francis, London, pp p13–p151

    Google Scholar 

  • Horvarth EM, Burgel JL, Messner K (1995) The production of soluble antifungal metabolites by the biocontrol fungus Trichoderma harzianum in connection with the formation of conidiospores. Mat Org 29:1–4

    Google Scholar 

  • Howell CR (1991) Biological control of Pythium damping off of cotton with seed coating preparations of Gliocladium virens. Phytopathology 81:738–741

    Google Scholar 

  • Howell CR (1998) The role of antibiosis in biocontrol. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol 2, Enzymes, Biological Control and Commercial Application. Taylor and Francis Ltd., London, pp 173–183

    Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    CAS  PubMed  Google Scholar 

  • Howell CR, Stipanovic RD (1994) Effect of sterol biosynthesis inhibitors on phytotoxin (viridiol) production by Gliocladium virens in culture. Phytopathology 84:969–972

    CAS  Google Scholar 

  • Howell CR, Stipanovic RD, Lumsden RD (1993) Antibiotic production by Strains of Gliocladium virens and its relation to the biocontrol of cotton seedling disease. Biocontrol Sci Tech 3:435–441

    Google Scholar 

  • Huang Q, Tezuka Y, Hatanaka Y et al (1995) Studies on metabolites of mycoparasitic fungi. IV. Minor peptaibols of Trichoderma koningii. Chem Pharm Bull 43:1663–1667

    CAS  Google Scholar 

  • Hynes J, Muller CT, Jones TH et al (2007) Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol 33:43–57

    CAS  PubMed  Google Scholar 

  • Iida AS, Shingu UT, Okuda M et al (1993) Fungal metabolites. Part 6. Nuclear magnetic study of antibiotic peptides, trichosporin Bs, from Trichoderma polysporum. J Chem Soc Perkin Trans 1:367–373

    Google Scholar 

  • Iida A, Sanekata M, Fujita T et al (1994) Fungal metabolites. XVI. Structures of new peptaibols, trichokindins I-VII, from the fungus Trichoderma harzianum. Chem Pharm Bull 42:1070–1075

    CAS  Google Scholar 

  • International Food Biotechnology Council (1990) Biotechnolgies and food: assuring the safety of foods produced by genetic modification. Regul Toxicol Pharmacol 12:S1–196

    Google Scholar 

  • Irmscher G, Jung G (1977) The hemolytic properties of the membrane modifying peptide antibiotics alamethicin, suzukacillin and trichotoxin. Eur J Biochem 80(1):165–174

    CAS  PubMed  Google Scholar 

  • Jacobsen BJ, Backman PA (1993) Biological and cultural plant disease controls: alternatives and supplements to chemicals in IPM systems. Plant Dis 77:311–315

    Google Scholar 

  • Jelen HH (2003) Use of solid phase microextraction (SPME) for profiling fungal volatile metabolites. Lett Appl Micro 36:263–267

    CAS  Google Scholar 

  • Jeleń H, Błaszczyk L, Chełkowski J et al (2014) Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycol Prog 13:589–600

    Google Scholar 

  • John STJ, Wicks JS, Hunt et al (2008) Colonisation of grapevine wood by Trichoderma harzianum and Eutypa lata. Aust J Grape Wine Res 14:18–24

    Google Scholar 

  • Jors E, Morant RC, Aguilar GC et al (2006) Occupational pesticide intoxications among farmers in Bolivia: a cross-sectional study. Environ Health: Glob Access Sci Source 5:10

    Google Scholar 

  • Joshi BB, Bhatt RP, Bahukhandi D (2010) Antagonistic and plant growth activity of Trichoderma isolates of Western Himalayas. J Environ Biol 31(6):921–992

    CAS  PubMed  Google Scholar 

  • Jung G, Konig WA, Leibfritz D et al (1976) Structural and membrane modifying properties of suzukacillin, a peptide antibiotic related to alamethicin. Part A. Sequence and conformation. Biochim Biophys Acta 45:164–181

    Google Scholar 

  • Kamal A, Akhtar R, Qureshi AA (1971) Biochemistry of microorganisms XX. 2,5-Dimethoxybenzoquinone, tartonic acid, itaconic acid, succinic acid, pyrocalciferol, epifriedelinol, lantosta-7,9 (11), 24-triene-3 β,21-diol, trichdermene A, methyl 2,4,6-octatriene and cordycepic acid, Trichoderma metabolites. Pak J Sci Ind Res 14:71–78

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kawada M, Yoshimoto Y, Kumagai H (2004) PP2A inhibitors, harzianic acid and related compounds produced by fungus strain F-1531. J Antibiot 57:235–237

    CAS  Google Scholar 

  • Kessler D (1992) FDA proposed statement of policy clarifying the regulation of food derived from genetically modified plants DECISION, www.biointegrity.org. 20 Mar 1992

  • Keswani C, Mishra S, Sarma BK et al (2014) Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Appl Microbiol Biotechnol 98:533–544

    CAS  PubMed  Google Scholar 

  • Keszler A, Forgacs E, Kotai L et al (2000) Separation and identification of volatile components in the fermentation broth of Trichoderma atroviride by solid phase extraction and gas chromatography-mass spectrometry. J Chromatogr Sci 38:421–424

    CAS  PubMed  Google Scholar 

  • Killham K (1994) Soil ecology. Cambridge University Press, Cambridge, p 242

    Google Scholar 

  • King RR, Calhoun LA (2009) The thaxtomin phytotoxins: sources, synthesis, biosynthesis, biotransformation and biological activity. Phytochemistry 70:833–841

    CAS  PubMed  Google Scholar 

  • Kleinkauf H, Rindfleisch H (1975) Non-ribosomal biosynthesis of the cyclic octadecapeptide alamethicin. Acta Microbiol Acad Sci Hung 22(4):411–418

    CAS  PubMed  Google Scholar 

  • Kobayashi M, Uehara H, Matsunami K et al (1993) A new polyketide produced by the imperfect fungus Trichoderma harzianum separated from the marine sponge Micale Cecilia. Tetrahedron Lett 34(49):7925–7928

    CAS  Google Scholar 

  • Komon-Zelazowska M, Bissett J, Zafari D et al (2007) Genetically closely related but phenotypically divergent Trichoderma species cause green mold disease in oyster mushroom farms worldwide. Appl Environ Microbiol 73:7415–7426

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kono Y, Knoche HW, Daly JM (1981) Structure of host–specific toxin. In: Durbin RD (ed) Toxins in plant diseases. Academic Press, New York, pp 221–257

    Google Scholar 

  • Korpi A, Jarnberg J, Pasanen AL (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193

    CAS  PubMed  Google Scholar 

  • Kredics L, Antal Z, Manczinger L et al (2001) Breeding of mycoparasitic Trichoderma strains for heavy metal resistance. Let Appl Microbiol 33:112–116

    CAS  Google Scholar 

  • Kroken S, Glass NL, Taylor JW et al (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and Saprobic ascomycetes. Proc Natl Acad Sci U S A 100:15670–15675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kubicek CP, Harman GE (eds) (1998) Trichoderma and Gliocladium. Taylor & Francis Ltd., London

    Google Scholar 

  • Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9(10):753–763

    PubMed  PubMed Central  Google Scholar 

  • Kubicek C, Herrera-Estrella A, Seidl-Seiboth V et al (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar K, Amaresan N, Bhagat S et al (2012) Isolation and characterization of Trichoderma spp. for antagonistic activity against root rot and foliar pathogens. Indian J Microbiol 52(2):137–144

    CAS  PubMed  Google Scholar 

  • Kumeda Y, Asao T, Lida A et al (1994) Effects of ergokonin produced by Trichoderma viride on the growth and morphological development of fungi. Bokin Bobai 22:663–670

    CAS  Google Scholar 

  • Lang B, Lia J, Zhoua X et al (2015) Koninginins L and M, two polyketides from Trichoderma koningii 8662. Phytochem Lett 11:1–4

    CAS  Google Scholar 

  • Leclerc G, Rebuffat S, Bodo B (1998) Directed biosynthesis of peptaibol antibiotics in two Trichoderma strains II Structure elucidation. J Antibiot 51:178–183

    CAS  Google Scholar 

  • Lee IH, Cho Y, Lehrer RI (1997a) Effects of pH and salinity on the antimicrobial properties of clavanins. Infect Immun 65:2898–2903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee IH, Cho Y, Lehrer RI (1997b) Styelins, broad-spectrum antimicrobial peptides from the solitary tunicate, Styela clava. Comp Biochem Physiol B 118:515–521

    CAS  PubMed  Google Scholar 

  • Leong J (1986) Siderophores: their biochemistry and possible role in the biocontrol of plant pathogens. Annu Rev Phytopathol 24:187–209

    CAS  Google Scholar 

  • Lepe MR, Ramírez-Suero M (2012) Biological control of mosquito larvae by Bacillus thuringiensis subsp. israelensis. In: Perveen F (ed) Insecticides – pest engineering. InTech, Rijeka, pp 239–264

    Google Scholar 

  • Lida J, Lida A, Takashashi Y et al (1993) Fungal metabolites. Part 5 Rapid structure elucidation of antibiotic peptides, minor components of trichosporins Bs from Trichoderma polysporum. Application of linked scan and continuous-flow fast- atom bombardment mass spectrometry. J Chem Soc Perkin Trans 1:357–365

    Google Scholar 

  • Liss SN, Brewer D, Taylor A et al (1985) Antibiotic activity of an isocyanide metabolite of Trichoderma hamatum against rumen bacteria. Can J Microbiol 31(9):767–772

    CAS  PubMed  Google Scholar 

  • Lopes FA, Steindorff AS, Geraldine AM et al (2012) Biochemical and metabolic profiles of Trichoderma strains isolated from common bean crops in the Brazilian Cerrado and potential antagonism against Sclerotinia sclerotiorum. Fungal Biol 116(7):815–824

    CAS  PubMed  Google Scholar 

  • Lorito M (1998) Chitinolytic enzymes and their genes. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium. Wiley, London, pp 87–115

    Google Scholar 

  • Lorito M, Harman GE, Hayes CK et al (1993) Chitynolytic enzymes produced by Trichoderma harzianum: antifungal activity of purified endochitinase and chitobiase. Phytopathology 83:302–307

    CAS  Google Scholar 

  • Lorito M, Hayes CK, di Pietro et al (1994) Purification, characterization and synergistic activity of a glucan 1,3-ß-glucosidase and N-acetyl-ß- glucosaminidase from Trichoderma harzianum. Phytopathology 84:398–405

    CAS  Google Scholar 

  • Lorito M, Farkas V, Rebuffat S (1996) Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J Bacteriol 178:6382–6385

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lorito M, Woo SL, García et al (1998) Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc Natl Acad Sci U S A 95:7860–7865

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JM (1990) Fungi as antagonists. In: Baker RR, Dunn PE (eds) New directions in biological control: alternatives for suppressing agricultural pests and diseases. Alan R. Liss, New York, pp 243–253

    Google Scholar 

  • Mandel W, Hayakawa H, Danzig R et al (1971) Evaluation of sinoatrial node function in man by overdrive suppression. Circulation 44:59–66

    CAS  PubMed  Google Scholar 

  • Mandels M (1975) Microbial sources of cellulase. Biotechnol Bioeng Symp 5:81–105

    CAS  Google Scholar 

  • Mann R, Rehm HJ (1976) Degradation products from aflatoxin B1 by Corynebacterium rubrum, Aspergillus niger, Trichoderma viride and Mucor ambiguus. Eur J Appl Microbiol 2:297–306

    CAS  Google Scholar 

  • Maroni M, Fanetti AC, Metruccio F (2006) Risk assessment and management of occupational exposure to pesticides in agriculture. Med Lav 97(2):430

    CAS  PubMed  Google Scholar 

  • Mathivanan N, Srinivasan K, Chelliah S (2000) Biological control of soil-borne diseases of cotton, eggplant, okra and sun Xower by Trichoderma viride. J Plant Dis Prot 107:235–244

    Google Scholar 

  • Mathivanan N, Prabavathy VR, Vijayanandraj VR (2008) The effect of fungal secondary metabolites on bacterial and fungal pathogens. In: Karlovsky P (ed) Secondary metabolites in soil ecology. Soil biology. Springer, Berlin, pp 129–140

    Google Scholar 

  • McCauley CD, Drath WH, Palus CJ et al (2006) The use of constructive-developmental theory to advance the understanding of leadership. Leadersh Q 17:634–653

    Google Scholar 

  • McGlacken GP, Fairlamb IJS (2005) 2-Pyrone natural products and mimetics: isolation, characterisation and biological activity. Nat Prod Rep 22:369–385

    CAS  PubMed  Google Scholar 

  • McIntyre M, Nielsen J, Arnau J et al (2004) Proceedings of the 7th European conference on fungal genetics, Copenhagen

    Google Scholar 

  • McSpadden Gardener B, Fravel D (2002) Biological control of plant pathogens: research commercialization, and application in the USA. Online Plant Health Prog. doi:10.1094/PHP-2002-0510-01-RV

    Article  Google Scholar 

  • Meruva NK, Penn JM, Farthing DE (2004) Rapid identification of microbial VOCs from tobacco molds using closed-loop stripping and gas chromatography/time-of flight mass spectrometry. J Ind Micro Biotechnol 31:482–488

    CAS  Google Scholar 

  • Meyer CE (1966) U-21,963, a new antibiotic. II. Isolation and characterization. Appl Microbiol 14:511–512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer CE, Reusser F (1967) A polypeptide antibacterial agent from Trichoderma viride. Experientia 23:85–86

    CAS  PubMed  Google Scholar 

  • Migheli Q, Gonzalez-Candelas L, Dealessi L (1998) Transformants of Trichoderma longibrachiatum overexpressing the beta-1,4-endoglucanase gene egl1 show enhanced biocontrol of Pythium ultimum on cucumber. Phytopathology 88:673–677

    CAS  PubMed  Google Scholar 

  • Moffatt JS, Bu’Lock JD, Yuen TH (1969) Viridiol, a steroid-like product from Trichoderma viride. J Chem Soc Chem Commun 14:839

    Google Scholar 

  • Mohamed-Benkada M, Montagu M, Biard JF et al (2006) New short peptaibols from a marine Trichoderma strain. Rapid Commun Mass Spectrom 20:1176–1180

    CAS  PubMed  Google Scholar 

  • Molle G, Doclohier H, Spach G (1987) Voltage dependent and multistate ionic channels induced by trichorzianines, antifungal peptides related to alamethicin. FEES Lett 224:208–212

    CAS  Google Scholar 

  • Mondéjar RL, Ros M, Pascual JA (2011) Mycoparasitism-related genes expression of Trichoderma harzianum isolates to evaluate their efficacy as biological control agent. Biol Control 56:59

    Google Scholar 

  • Monte E (2001) Understanding Trichoderma: between agricultural biotechnology and microbial ecology. Int Microbiol 4:1–4

    CAS  PubMed  Google Scholar 

  • Moss MO, Jackson RM, Rodgers D (1975) The characterization of 6-pent-1-enyl) pyrone from Trichoderma viride. Phytochemistry 14:2706–2708

    CAS  Google Scholar 

  • Mukherjee PK (2011) Genomics of biological control–whole genome sequencing of two mycoparasitic Trichoderma spp. Curr Sci 101(3):10

    Google Scholar 

  • Mukherjee PK, Horwitz BA, Kenerley CM (2012a) Secondary metabolism in Trichoderma: a genomic perspective. Microbiology 158:35–45

    CAS  PubMed  Google Scholar 

  • Mukherjee PK, Buensanteai N, Moran-Diez ME et al (2012b) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 158:155–165

    CAS  PubMed  Google Scholar 

  • Muller A, Faubert P, Hagen M et al (2013) Volatile profiles of fungi – chemotyping of species and ecological functions. Fungal Genet Biol 54:25–33

    PubMed  Google Scholar 

  • Mumpuni A, Sharma HS, Brown AE et al (1998) Effect of metabolites produced by Trichoderma harzianum biotypes and Agaricus bisporus on their respective growth radii in culture. Appl Environ Microbiol 64:5053–5056

    CAS  PubMed  PubMed Central  Google Scholar 

  • Narayanan K (2004) Insect defense: its impact on microbial control of insect pests. Curr Sci 86(6):25

    Google Scholar 

  • Nemc ovic M, Farkas V (2008) Induction of condition by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett 284:231–236

    Google Scholar 

  • Nene YL, Thapliyal PN (1993) Evaluation of fungicides. In: Fungicides in plant disease control. Oxford and IBH Publishing Company, New Delhi, p 531

    Google Scholar 

  • Neuhof T, Dieckmann R, Druzhinina IS et al (2007) Intact-cell MALDI-TOF mass spectrometry analysis of peptaibol formation by the genus Trichoderma/Hypocrea: can molecular phylogeny of species predict peptaibol structures? Microbiology 153:3417–3437

    CAS  PubMed  Google Scholar 

  • New AP, Eckers C, Haskins NJ et al (1996) Structures of polysporins A-D, four new peptaibols isolated from Trichoderma polysporum. Tetrahedron Lett 37:3039–3042

    CAS  Google Scholar 

  • Nikolajeva V, Petrina Z, Vulfa L et al (2012) Growth and antagonism of Trichoderma spp. and conifer pathogen Heterobasidion annosum s.l. in vitro at different temperatures. Adv Microbiol 2:295–302

    Google Scholar 

  • Oh SU, Lee SJ, Kim JH (2000) Structural elucidation of new antibiotic peptides, atroviridins A, B, and C from Trichoderma atroviride. Tetrahedron Lett 41:61–64

    CAS  Google Scholar 

  • Omero C, Inbar J, Rocha-Ramirez V et al (1999) G protein activators and cAMP promote mycoparasitic behaviour in Trichoderma harzianum. Mycol Res 103:1637–1642

    CAS  Google Scholar 

  • Ordentlich A, Wiesman Z, Gottlieb HE et al (1992) Inhibitory furanone produced by the biocontrol agent Trichoderma harzianum. Phytochemistry 31:485–486

    CAS  Google Scholar 

  • Osbourn A (2010) Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet 26:449–457

    CAS  PubMed  Google Scholar 

  • Overton BE, Stewart EL, Geiser DM et al (2006) Systematics of Hypocrea citrina and related taxa. Stud Mycol 56:1–38

    PubMed  PubMed Central  Google Scholar 

  • Pakdaman N, Ghaderian SM, Ghasemi R et al (2013) Effects of calcium/magnesium quotients and nickel in the growth medium on growth and nickel accumulation in Pistacia atlantica. J Plant Nutr 36:1708–1718

    CAS  Google Scholar 

  • Pandey RC, Cook JC, Rinehart KL Jr (1977) High resolution and field desorption mass spectrometry studies and revised structures of alamethicins I and II. J Am Chem Soc 99:8469–8483

    CAS  Google Scholar 

  • Papavizas GG (1985) Trichoderma and Gliocladium: biology, ecology and potential for biocontrol. Ann Rev Phytopathol 23:23–54

    Google Scholar 

  • Patil AS, Lunge AG (2012) Strain improvement of Trichoderma harzianum by UV mutagenesis for enhancing it’s biocontrol potential against aflotoxigenic Aspergillus species. Exp 2:228–242

    Google Scholar 

  • Paulitz TC (2000) Population dynamics of biocontrol agents and pathogens in soils and rhizospheres. Euro J Plant Pathol 106:401–413

    Google Scholar 

  • Pimentel D, Greiner A (1997) Environmental and socio-economic costs of pesticide use. In: Pimentel D (ed) Techniques for reducing pesticide use: environmental and economic benefits. Wiley, Chichester, pp 51–78

    Google Scholar 

  • Pinches SE, Apps P (2007) Production in food of 1, 3-pentadiene and styrene by Trichoderma species. Int J Food Microbiol 116:182–185

    CAS  PubMed  Google Scholar 

  • Pittendrigh BR, Gaffney PJ (2001) Pesticide resistance: can we make it a renewable resource? J Theor Biol 211:365–375

    CAS  PubMed  Google Scholar 

  • Polizzi G, Cirvilleri G, Catara A (2002) Longstanding experience in defense fungicides on grapevine in Sicily made with chemical and biological. ATTI Giornate Fitopatologiche 2:381–388

    Google Scholar 

  • Polizzi V, Adams A, Malysheva SV et al (2012) Identification of volatile markers for indoor fungal growth and chemotaxonomic classification of Aspergillus species. Fungal Biol 116:941–953

    CAS  PubMed  Google Scholar 

  • Pratt BH, Sedgley JH, Heather WA (1972) Oospore production in Phytophtora cinnamomi in the presence of Trichoderma koningii. Aust J Biol Sci 25:861–863

    Google Scholar 

  • Punja ZK, Utkhede RS (2003) Using fungi and yeasts to manage vegetable crop diseases. Trends Biotechnol 21:400–407

    CAS  PubMed  Google Scholar 

  • Pyke TR, Dietz A (1966) U-21,963, a new antibiotic. I. Discovery and biological activity. Appl Microbiol 14:506–510

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qi W, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53(4):355–364

    CAS  PubMed  Google Scholar 

  • Rahman MF, Begum MF, Alam MF (2009) Screening of Trichoderma isolates as a biological control agent against Ceratocystis paradoxa causing pineapple disease of sugarcane. Mycoscience 37(4):277–285

    CAS  Google Scholar 

  • Rajappan K, Raguchander T, Manickam K (1996) Efficacy of UV-induced mutants of Trichoderma viride against Sclerotia rolfesii. Plant Dis Res 11:97–99

    Google Scholar 

  • Rajput RB, Solanky KU, Prajapati VP et al (2013) Effect of fungal and bacterial bioagents against Alternaria alternata (fr.) Keissler in vitro condition. Bioscan 8(2):627–629

    CAS  Google Scholar 

  • Ratnakumari YR, Nagamani A, Bhramaramba S et al (2011) Non-volatile and volatile metabolites of antagonistic Trichoderma against collar rot pathogen of Mentha arvensis. Int J Pharm Biomed Res 2(2):56–58

    Google Scholar 

  • Rebuffat S, Prigent Y, Guette A et al (1991) Tricholongins BI and BII 19-residue peptaibols from Trichoderma longibrachiatum. Solution structure from two dimensional NMR spectroscopy. Eur J Biochem 201:661–674

    CAS  PubMed  Google Scholar 

  • Rebuffat S, Duclohier H, Auvin-Guette C et al (1992) Membrane-modifying properties of the pore-forming peptaibols saturnisporin SA IV and harzianin HA V. FEMS Microbiol Immunol 105:151–160

    Google Scholar 

  • Rebuffat S, Conraux L, Massias M et al (1993) Sequence and solution conformation of the 20-residue peptaibols, saturnisporins SA II and SA IV. Int J Pept Prot Res 41(1):74–84

    CAS  Google Scholar 

  • Rebuffat S, Goulard C, Bodo B (1995) Antibiotic peptides from Trichoderma harzianum: harzianins HC, proline-rich 14-residue peptaibols. J Chem Soc 1:1849–1855

    Google Scholar 

  • Rebuffat S, Hlimi S, Prigent Y et al (1996) Isolation and structural elucidation of the 11- residue peptaibol antibiotic harzianin HK VI. J Chem Soc Perkins Trans 16:2021–2027

    Google Scholar 

  • Rebuffat S, Goulard C, Hlimi S et al (2000) Two unprecedented natural Aib-peptides with the (Xas-Yaa-Aib-Pro) motif and an unusual C-terminus: Structures, membrane-modifying and antibacterial properties of pseudokonins KLIII and KL VI from fungus Trichoderma pseudokoningii. J Pept Sci 6:519–533

    CAS  PubMed  Google Scholar 

  • Reeves RJ, Jackson RM (1972) Induction of Phytophthora cinnamomi oospores in soil by Trichoderma viride. Trans Br Mycol Soc 59:156–159

    Google Scholar 

  • Reino JL, Guerrero RF, Hernandez-Galan R et al (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123

    CAS  Google Scholar 

  • Reithner B, Brunner K, Schuhmacher R et al (2005) The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet Biol 42(9):749–760

    CAS  PubMed  Google Scholar 

  • Reithner B, Schuhmacher R, Stoppacher N et al (2007) Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet Biol 44(11):1123–1133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rey M, Delgado JJ, Rincon AM et al (2000) Improvement of Trichoderma strains for biocontrol. Micol Ind Mico 17:531–536

    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

    CAS  PubMed  Google Scholar 

  • Ritieni A, Fogliano V, Nanno D et al (1995) Paraceksin E a new peptaibol from Trichoderma satumisporum. J Nat Prod 296:1745–1748

    Google Scholar 

  • Rocha-Ramirez V, Omero C, Chet I et al (2002) Trichoderma atroviride G-protein a-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot Cell 1:594–605

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roco A, Perez LM (2001) In vitro biocontrol activity of Trichoderma harzianum on Alternaria alternata in the presence of growth regulators. Electron J Biotechnol 4(2):1–6. ISSN, 0717-3458

    Google Scholar 

  • Rossoni RD, Barbosa JO, De Oliveira FE et al (2014) Biofilms of Candida albicans serotypes A and B differ in their sensitivity to photodynamic therapy. Lasers Med Sci 29(5):1679–1684

    PubMed  Google Scholar 

  • Rubio MB, Hermosa R, Reino JL et al (2009) Thctf1 transcription factor of Trichoderma harzianum is involved in 6- pentyl-2H-pyran-2-one production and antifungal activity. Fungal Genet Biol 46:17–27

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Sailaja N, Chandrasekhar M, Rekhadevi P et al (2006) Genotoxic evaluation of workers employed in pesticide production. Mutat Res 609(1):74–80

    CAS  PubMed  Google Scholar 

  • Sakuno E, Yabe K, Hamasaki T (2000) New inhibitor of 5′-hydroxyaverantin dehydrogenase, an enzyme involved in aflatoxin biosynthesis, from Trichoderma hamatum. J Nat Prod 63:1677–1678

    CAS  PubMed  Google Scholar 

  • Samuels GJ (1996) Trichoderma: a review of biology and systematics of the genus. Mycol Res 100:923–935

    Google Scholar 

  • Samuels GJ (2006) Trichoderma: systematics, the sexual state and ecology. Phytopathology 96:195–206

    CAS  PubMed  Google Scholar 

  • Sawa R, Mori Y, Iinuma H et al (1994) Harzianic acid, a new antimicrobial antibiotic from a fungus. J Antibiot 47:731–732

    CAS  Google Scholar 

  • Scarselletti R, Faull JL (1994) In Vitro activity of 6-pentyl- a-pyrone, a metabolite of Trichoderma harzianum, in the inhibition of Rhizoctonia solani and Fusarium oxysporum f. sp. lycopersici. Mycol Res 98:1207–1209

    CAS  Google Scholar 

  • Scheuer PJ (1992) Isocyanides and cyanides as natural products. Acc Chem Res 25:433–439

    CAS  Google Scholar 

  • Schirmbock M, Lorito M, Wang YL et al (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60:4364–4370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schroeckh V, Scherlach K, Nützmann HW (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106:14558–14563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert M, Fink S, Schwarze WMR (2008) In vitro screening of an antagonistic Trichoderma strain against wood decay fungi. Arboric J 31:227–248

    Google Scholar 

  • Schwab EK, Keller NP (2008) Regulation of secondary metabolite production in filamentous ascomycetes. Mycol Res 112:225–230

    Google Scholar 

  • Score AJ, Palfreyman JW (1994) and Biological control of the dry rot fungus Serpula lacrymans by Trichoderma species: the effects of complex and synthetic media on interaction and hyphal extension rates. Int Biodeterior Biodegrad 33:115–128

    Google Scholar 

  • Serrano-Carreon L, Hathout Y, Bensoussan M et al (1993) Metabolism of linoleic acid or mevalonate and 6-pentyl-α-pyrone biosynthesis by Trichoderma species. Appl Environ Microbiol 59:2945–2950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shahbazi S, Ispareh K, Karimi M et al (2014) Gamma and UV radiation induced mutagenesis in Trichoderma reesei to enhance cellulases enzyme activity. IJFAS 3(5):543–554

    Google Scholar 

  • Sharma A, Johri BN, Sharma AK et al (2003) Plant growth promoting bacterium Pseudomonas sp., strain GFP (3) influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol Biochem 35:887–894

    CAS  Google Scholar 

  • Sharma K, Kumar M, Misra RM (2009) Morphological, biochemical and molecular characterization of Trichoderma harzianum isolates for their efficacy as biocontrol agents. J Phytopathol 157:51–56

    CAS  Google Scholar 

  • Sharman GJ et al (1996) Structural elucidation of XR586, a peptaibol -like antibiotic from Acremonium persicinum. Biochem J 320(3):723–728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sherman DH (2002) New enzymes for “warheads”. Nat Biotechnol 20:984–985

    CAS  PubMed  Google Scholar 

  • Siddiquee S, Cheong BE, Taslima K (2012) Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J Chromatogr Sci 50:358–367

    CAS  PubMed  Google Scholar 

  • Simon A, Dunlop RW, Ghisalberti EL et al (1988) Trichoderma koningii produces a pyrone compound with antibiotic properties. Soil Biol Biochem 20:263–264

    CAS  Google Scholar 

  • Singh J, Faull JL (1988) Antagonism and biological control. In: Mukerji KG, Garg KL (eds) Biocontrol of plant diseases, vol 2. CRC Press, Boca Raton, pp 167–177

    Google Scholar 

  • Singh RS, Saini GK, Kennedy JF (2010) Maltotriose syrup preparation from pullulan using pullulanase. Carbohydr Polym 80:401–407

    CAS  Google Scholar 

  • Singh SK, Strobel GA, Knighton B et al (2011) An endophytic Phomopsis sp. possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61:729–739

    PubMed  Google Scholar 

  • Sivasithamparam K, Ghisalberti EL (1998) Secondary metabolism in Trichoderma and Gliocladium. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium. Taylor & Francis Ltd., London, pp p139–p191

    Google Scholar 

  • Skidmore AM, Dickinson CM (1976) Colony interactions and hyphal interference between Sepatoria nodorum and phylloplane fungi. Trans Br Mycol Soc 66:57–64

    Google Scholar 

  • Sodeoka M, Sampe R, Kojima S (2001) Asymmetric synthesis of a 3-acyltetronic acid derivative, RK-682, and formation of its calcium salt during silica gel column chromatography. Chem Pharm Bull 49:206–212

    CAS  Google Scholar 

  • Solfrizzo M, Altomare C, Visconti A et al (1994) Detection of peptaibols and their hydrolysis products in cultures of Trichoderma species. Nat Toxins 2:360–365

    CAS  PubMed  Google Scholar 

  • Steyaert M, Vanaverbeke J, Vanreusel A et al (2003) The importance of fine-scale, vertical profiles in characterizing nematode community structure. Estuar Coast Shelf Sci 58:353–366

    Google Scholar 

  • Stoate C, Boatman ND, Borralho RJ et al (2001) Ecological impacts of arable intensification in Europe. J Environ Manage 63:337–365

    CAS  PubMed  Google Scholar 

  • Stoessl A (1981) Structure and biogenetic relations: fungal nonhost-specific. In: Durbin RD (ed) Toxins in plant diseases. Academic press, New York, pp 109–219

    Google Scholar 

  • Sun F, Zhang W, Hu H et al (2008) Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol 146:178–188

    CAS  PubMed  PubMed Central  Google Scholar 

  • Szekeres A, Leitgeb B, Kredics L et al (2005) Peptaibols and related peptaibiotics of Trichoderma. Acta Microbiol Immunol Hung 52:137–168

    CAS  PubMed  Google Scholar 

  • Tamura A, Kotani H, Naruto S (1975) Trichoviridin and dermadin from Trichoderma sp. TK-1. J Antibiot 28:161–162

    CAS  Google Scholar 

  • Tanaka H, Kuroda A, Marusawa H et al (1987) Structure of FK506, a novel immunosuppressant isolated from Streptomyces. J Am Chem Soc 109(16):5031–5033

    CAS  Google Scholar 

  • Tarus PK, Lang’at-Thoruwa CC, Wanyonyi AW (2003) Bioactive metabolites from Trichoderma harzianum and Trichoderma longibrachiatum. Bull Chem Soc Ethiop 17(2):185–190

    CAS  Google Scholar 

  • Thines E, Anke H, Weber RW (2004) Fungal secondary metabolites as inhibitors of infection-related morphogenesis in phytopathogenic fungi. Mycol Res 108:14–25

    CAS  PubMed  Google Scholar 

  • Thrane U, Poulsen SB, Nirenberg HI et al (2001) Identification of Trichoderma strains by image analysis of HPLC chromatograms. FEMS Microbiol Lett 203:249–255

    CAS  PubMed  Google Scholar 

  • Van Lancker F, Adams A, Delmulle B et al (2008) Use of headspace SPME-GC-MS for the analysis of the volatiles produced by indoor molds grown on different substrates. J Environ Monit 10:127–133

    Google Scholar 

  • Verma M, Brar SK, Tyagi RD et al (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20

    Google Scholar 

  • Vinale F, Marra R, Scala F et al (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148

    CAS  PubMed  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL et al (2008a) Trichoderma plant pathogen interactions. Soil Biol Biochem 40:1–10

    CAS  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL et al (2008b) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    CAS  Google Scholar 

  • Vinale F, Ghisalberti EL, Sivasithamparam K (2009a) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48:705–711

    CAS  PubMed  Google Scholar 

  • Vinale F, Flematti G, Sivasithamparam K et al (2009b) Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J Nat Prod 72:2032–2035

    CAS  PubMed  Google Scholar 

  • Vinale F, Arjona GI, Nigro M et al (2012) Cerinolactone, a hydroxylactone derivative from Trichoderma cerinum. J Nat Prod 75:103–106

    CAS  PubMed  Google Scholar 

  • Vinale F, Nigro M, Sivasithamparam K et al (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347(2):123–129

    CAS  PubMed  Google Scholar 

  • Vinale F, Manganiello G, Nigro M et al (2014) Novel fungal metabolite with beneficial properties for agricultural applications. Molecules 19:9760–9772

    PubMed  PubMed Central  Google Scholar 

  • Viterbo A, Ramot O, Chemin LY et al (2002) Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens. A Van Leeuw J Microbiol 81:549–556

    CAS  Google Scholar 

  • Wardle DA, Parkinson D, Waller JE (1993) Interspecific competitive interactions between pairs of fungal species in natural substrates. Oecologia 94:165–172

    CAS  PubMed  Google Scholar 

  • Weindling R (1932) Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22:837–845

    Google Scholar 

  • Weindling R, Emerson OH (1936) The isolation of a toxic substance from the culture filtrate of Trichoderma. Phytopathology 26:1068–1070

    CAS  Google Scholar 

  • Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int Biodeterior Biodegrad 39:199–205

    CAS  Google Scholar 

  • Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511

    CAS  PubMed  Google Scholar 

  • WHO (1992) Cadmium. Environmental Health Criteria, vol 134, Geneva

    Google Scholar 

  • Wiest A, Grzegorski D, Xu BW et al (2002) Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem 277:20862–20868

    CAS  PubMed  Google Scholar 

  • Wilhite SE, Lumsden RD, Straney DC (2001) Peptide synthetase gene in Trichoderma virens. Appl Environ Microbiol 67:5055–5062

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wipf P, Kerekes AD (2003) Structure reassignment of the fungal metabolite TAEMC161 as the phytotoxin viridiol. J Nat Prod 66:716–871

    CAS  PubMed  Google Scholar 

  • Woo SL, Lorito M (2007) Exploiting the interactions between fungal antagonists, pathogens and the plant for biocontrol. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. IOS, Springer Press, Amsterdam, pp 107–130

    Google Scholar 

  • Worasatit N, Sivasithamparam K, Ghisalberti EL et al (1994) Variation in pyrone production, pectic enzymes and control of rhizoctonia root rot of wheat among single-spore isolates of Trichoderma koningii. Mycol Res 98:1357–1363

    CAS  Google Scholar 

  • Yamaguchi Y, Manita D, Takeuchi T et al (2010) Novel terpenoids, Trichodernoic acid A and B isolated from Trichoderma virens, are selective inhibitors of family X DNA polymerases. Biosci Bitechnol Biochem 74(4):793–801

    CAS  Google Scholar 

  • Youssef F, Roukas T, Biliaderis CG (1999) Pullulan production by a nonpigmented strain of Aureobasidium pullulans using batch and fed batch culture. Process Biochem 34:355–366

    CAS  Google Scholar 

  • Zeppa G, Allegrone G, Barbeni M et al (1990) Variability in the production of volatile metabolites by Trichoderma viride. Ann Micro 40:171–176

    CAS  Google Scholar 

  • Zhang M, Li N, Chen R et al (2014) Two terpenoids and a polyketide from the endophytic fungus Trichoderma sp. Xy24 isolated from mangrove plant Xylocarpus granatum. J Chin Pharm Sci 23(6):424–424

    CAS  Google Scholar 

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Acknowledgements

We express our heartfelt thanks for the financial assistance for postdoc (File no.F.30-100(SC)/2009(SA-II) extended to Prof. Anita Patil by UGC (University Grants Commission), government of India. We extend our thanks to the Department of Biotechnology, SGBAU for providing support to us.

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Authors and Affiliations

  1. Department of Biotechnology, Sant Gadge Baba Amravati University, Amravati, Maharashtra, 444 602, India

    Anita Surendra Patil

  2. College of Horticulture, Dr. Panjabrao Deshmukh Krishi Vidyapeeth, Akola, Maharashtra, 444 104, India

    Surendra Rajaram Patil

  3. Department of Forensic Biology, Govt. Institute of Forensic Science, Aurangabad, Maharashtra, 431004, India

    Hariprasad Madhukarrao Paikrao

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Correspondence to Anita Surendra Patil .

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  1. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Devendra K. Choudhary

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

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Patil, A.S., Patil, S.R., Paikrao, H.M. (2016). Trichoderma Secondary Metabolites: Their Biochemistry and Possible Role in Disease Management. In: Choudhary, D.K., Varma, A. (eds) Microbial-mediated Induced Systemic Resistance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-0388-2_6

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