ORIGINAL ARTICLE
Bioactivity of Trichoderma harzianum A peptaibols against Zymoseptoria tritici causal agent of septoria leaf blotch of wheat
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1
Department of Production, Protection, and Biotechnology, Hassan II Institute of Agronomic and Veterinary Medicine, Rabat, Morocco
2
Department of Veterinary, Hassan II Institute of Agronomic and Veterinary Medicine, Rabat, Morocco
3
FungiSem, IRHS, INRA-University of Angers-Agrocampus-Ouest, Angers, France
4
Laboratory of Phytopathology and Post-Harvest Quality, Regional Centre for Agronomic Research, Kénitra, Morocco
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2022-09-02
Acceptance date: 2022-10-27
Online publication date: 2022-09-03
Corresponding author
Ilham Barakat
Department of Production, Protection, and Biotechnology, Hassan II Institute of Agronomic and Veterinary Medicine,
Rabat, Morocco
Journal of Plant Protection Research 2023;63(1):59-67
HIGHLIGHTS
- In this study, we developed a novel method to evaluate the antibiosis effect of Trichoderma harzianum A through the use of the nephelometry technique. The results of our study confirmed the efficacy of the methodology adopted and the importance of this novel T. harzianum strain.
KEYWORDS
TOPICS
ABSTRACT
In this study Trichoderma harzianum strain A was isolated from the rhizosphere of an
argan tree in southern Morocco. Trichoderma harzianum strain A had previously demonstrated
a high antagonistic potential in vitro by direct confrontation and in vivo on wheat
plants in pots under greenhouse conditions against Zymoseptoria tritici, the agent of septoria
leaf blotch. In this study, the activity of filtrates prepared from the liquid culture of
T. harzianum A alone and from the confrontation medium with two Z. tritici strains [G1-1
(durum wheat) and A5-1 (soft wheat)] on the inhibition of Z. tritici pycnidiospore germination
was studied by nephelometry. The results of the antibiosis assay revealed that filtrate
0 (A in confrontation with G1-1) and F3 (A against A5-1) showed 95% of G1-1 and A5-1
pycnidiospore inhibition at 9/10 dilution of the undiluted filtrates after 4 days of incubation.
To understand and explain the antifungal activity of these filtrates, the extraction and
identification of secondary molecules of peptaibiotic nature secreted by T. harzianum A in
the three studied filtrates were performed. According to the results of high-performance
liquid chromatography-mass spectrometry (HPLC-MS) analyses, 38 peptaibiotic molecules
reported in the literature for their antifungal activity were identified in the different
extracts at high concentrations (high peak intensities). These molecules are divided
into nine groups, namely: Trichocryptin, Trichobrevin, Triochocryptin, Hypocompactin,
Hyporodicin, Trichocompactin, Alamethicine, Trichoferin, and Trichokonin. It was also
shown that the presence of the pathogen induces the production of peptaibols by the antagonistic
strain of Trichoderma.
ACKNOWLEDGEMENTS
The authors would like to thank the Ministry of National
Education, Vocational Training, Higher Education,
and Scientific Research of the Kingdom of
Morocco for funding the Arimnet research project
entitled “Bacplant,” and, we acknowledge the French
ANR (Agence National de la Recherche) project Lab
-Com, ESTIM for the financial support.
RESPONSIBLE EDITOR
Andrea Toledo
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (58)
1.
Almi H. 2016 Study of the Myco-Pathogens of Lens Culinaris and Evaluation of the Effect of Two Strains of Trichoderma harzianum: the Case of Fusarium and Cylindrosporiose. Mentouri, Algeria, 166 pp.
2.
Atanasova L., Druzhinina I.S., Jaklitsch W.M. 2013. Two hundred Trichoderma species recognized based on molecular phylogeny. p. 10–42. In: “Trichoderma: biology and applications” (Mukherjee P.K., Singh U.S., Horwitz B.A., Schmoll M., Mukherjee M., eds.). CABI Nosworthy Way Wallingford, Oxon, UK. DOI:
http://hdl.handle.net/20.500.1....
3.
Ayers S., Ehrmann B.M., Adcock A.F., Kroll D.J., Carcache de Blanco E.J., Shen Q., Swanson S.M., Falkinham J.O., Wani M.C., Mitchell S.M., Pearce C.J., Oberlies N.H. 2012. Peptaibols from two unidentified fungi of the order Hypocreales with cytotoxic, antibiotic, and anthelmintic activities. Journal of Peptide Science 18: 500–510. DOI: 10.1002/psc.2425.
4.
Bandani A.R., Amiri B., Butt T.M., Gordon-weeks R. 2001. Effects of efrapeptin and destruxin, metabolites of entomogenous fungi, on the hydrolytic activity of a vacuolar type ATPase identified on the brush border membrane vesicles of Galleria mellonella midgut and on plant membrane bound hydrolytic enzymes. Biochimica et Biophysica Acta 1510: 367–377. DOI: 10.1016/s0005-2736(00)00370-9.
5.
Barakat I., Chtaina N., El Guilli M., Ezzahiri B. 2018. Evaluation of antagonistic potential of some isolates of bacteria and Trichoderma spp. in the control of Zymoseptoria tritici causal agent of wheat leaf spot. Revue Marocaine des Sciences Agronomiques et Vétérinaires 6: 345–354.
6.
Barakat I., Chtaina N., El Guilli M., Ezzahiri B. 2019a. Efficacy of Bacillus amyloliquefaciens and Trichoderma harzianum as biocontrol agent of septoria of wheat by seed coating. Moroccan Journal of Plant Protection 13: 9–18.
7.
Barakat I., Chtaina N., Grappin P., El Guilli M., Ezzahiri B., Aligon S., Neveu M., Marchi M. 2019b. Induced Systemic Resistance (ISR) in Arabidopsis thaliana by Bacillus amyloliquefaciens and Trichoderma harzianum Used as Seed Treatments. Agriculture 9: 166. DOI: 10.3390/agriculture9080166.
8.
Benouzza S. 2012. Inventory of the Mycoflora of the Olive Rhizosphere and Study of its Antagonistic Potentialities Towards Verticillium dahliae Kelb: Agent of the Werticillium Wilt of the Olive Tree. Oran, Algeria, 150 pp.
9.
Berg A., Ritzau M., Ihn W., Schlegel B., Fleck W.F., Heinze S., Grafe U. 1996. Isolation and structure of bergofungin, a new antifungal peptaibol from Emericellopsis donezkii KI 0059. Journal of Antibiotics 49: 817–820. DOI: 10.7164/antibiotics.49.817.
10.
Blaszczyk L., Siwulski M., Sobieralski K., Lisiecka J., Jedrycaka M. 2014. Trichoderma spp. Application and prospects for use in organic farming and industry. Journal of Plant Protection Research 54: 309–317. DOI:
https://doi.org/10.2478/jppr-2....
11.
Boureghda H., Bouznad Z. 2009. Biological control of Fusarium wilt of chickpea using isolates of Trichoderma atroviride, T. harzianum and T. longibrachiatum. Acta Phytologica Entomologica Hungarica 44: 25–38. DOI: 10.1556/APhyt.44.2009.1.4.
12.
Brückner H., Becker D., Gams W., Degenkolb T. 2009. Aib and Iva in the biosphere: neither rare nor necessarily extraterrestrial. Chemistry Biodiversity 6: 38–56. DOI: doi.org/10.1002/cbdv.200800331.
13.
Bruckner H., Graf H. 1983. Paracelsin, a peptide antibiotic containing alpha-aminoisobutyric acid, isolated from Trichoderma reesei Simmons. Part A Experientia 39: 528–530.
14.
Carroux A., van Bohemen A.I., Roullier C., Robiou du Pont T., Vansteelandt M., Bondon A., Zalouk-Vergnoux A., Pouchus Y.F., Ruiz N. 2013. Unprecedented 17-residue peptaibiotics produced by marine-derived Trichoderma atroviride. Chemistry Biodiversity 10: 772–786. DOI: doi.org/10.1002/cbdv.201200398.
15.
Chet I. 1993. Biotechnology in Plant Disease Control. Wiley and Sons, New York, 373 pp.
16.
Crutcher F.K., Parich A., Schuhmacher R. 2013. A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genetic Biology 56: 67–77. DOI: 10.1016/j.fgb.2013.05.003.
17.
de la Cruz J., Hidalgo-Gallego A., Lora J.M., Benitez T., Pintor-Toro J.A., Llobell A. 1992. Isolation and characterization of three chitinases from Trichoderma harzianum. European Journal of Biochemistry 206: 859–867. DOI: 10.1111/j.1432-1033.1992.tb16994.x.
18.
Degenkolb T., Brückner H. 2008. Peptaibiomics: towards a myriad of bioactive peptide containing Cα-dialkylamino acids?. Chemistry Biodiversity 5: 1817–1843. DOI: 10.1002/cbdv.200890171.
19.
Degenkolb T., Von Dohren H., Nielsen K.F., Samuels G.J., Bruckner H. 2008. Recent advances and future prospects in peptaibiotics, hydrophobin, and mycotoxin research, and their importance for chemotaxonomy of Trichoderma and Hypocrea. Chemistry Biodiversity 5: 671–680. DOI: 10.1002/cbdv.200890064.
20.
Degenkolb T., Kirschbaum J., Bruckner H. 2007. New sequences, constituents, and producers of peptaibiotics: an updated review. Chemistry Biodiversity 4: 1052–1067. DOI: 10.1002/cbdv.200790096.
21.
Degenkolb T., Grafenhan T., Nirenberg H.I., Gams W., Bruckner H. 2006. Trichoderma brevicompactum Complex: Rich Source of Novel and Recurrent Plant-Protective Polypeptide Antibiotics (Peptaibiotics). Journal of Agriculture and Food Chemistry 54: 7047-7061.
22.
Dubey S.C., Suresh M., Singh B. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Conrol 40: 118–127. DOI: doi.org/10.1016/j.biocontrol.2006.06.006.
23.
Figueroa M., Raja H., Falkinham J.O., Adcock A.F., Kroll D.J., Wani M.C., Pearce C.J., Oberlies N.H. 2013. Peptaibols, tetramic acid derivatives, isocoumarins, and sesquiterpenes from a Bionectria sp. (MSX 47401). Journal of Natural Products 76: 1007–1015. DOI: 10.1021/np3008842.
24.
Geremia R.A., Goldma G.H., Jacobs D., Ardiles W., Vila S.B., Van Montagu M., Herrera-Estrella A. 1993. Molecular characterization of the proteinase-encoding gene, prb1, related to mycoparasitism by Trichoderma harzianum. Molecular Microbiology 8: 603–613. DOI: 10.1111/j.1365-2958.1993.tb01604.x.
25.
Ghisalberti E.L., Narbey M.J., Dewan M.M., Sivasithamparam K. 1990. Variability among strains of Trichoderma harzianum in their ability to reduce take-all and to produce pyrones. Plant Soil 121: 287–291. DOI: doi.org/10.1007/BF00012323.
26.
Harman G.E., Howell C.R., Viterbo A., Chet I., Lorito M. 2004. Trichoderma spp. – opportunistic avirulent plant symbionts. Nature Reviews Microbiology 2: 43–56. DOI: doi.org/10.1038/nrmicro797.
27.
Harman G.E. 2000. Myths and dogmas of biocontrol: changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Disease 84: 377–393. DOI:
https://doi.org/10.1094/PDIS.2....
28.
Jelen H., Blaszczyk L., Chelkowski J., Rogowicz K., Strakowska J. 2013. Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycological Progress 13: 589–600. DOI: doi.org/10.1007/s11557-013-0942-2.
29.
Kim C.S., Shirouzu T., Nakagiri A., Sotome K., Nagasawa E., Maekawa N. 2012. Trichoderma mienum sp. nov., isolated from mushroom farms in Japan. Antonie van Leeuwenhoek 102: 629–641. DOI: doi.org/10.1007/s10482-012-9758-3.
30.
Kim C.S., Shirouzu T., Nakagiri A., Sotome K., Nagasawa E., Maekawa N. 2013. Trichoderma eijii and T. pseudolacteum, two new species from Japan. Mycological Progress 12: 739–753. DOI: doi.org/10.1007/s11557-012-0886-y.
31.
Kim Y.H., Kim Y.S., Chae K.S., Kim K.S. 2000. Antiviral activity of antibiotic peptaibols, Chrysospermins B and D, produced by Apiocrea sp. 14T against TMV infection. Journal of Microbiology and Biotechnology 1: 522–528.
32.
Kimonyo A., Brückner H. 2013. Sequences of metanicins, 20-residue peptaibols from the ascomycetous fungus CBS 597.80. Chemistry Biodiversity 10: 813–826. DOI: 10.1002/cbdv.201300064.
33.
Landreau A., Pouchus Y.F., Sallenave-Namot C., Biard J.F., Boumard M.C., Du Pont T.R., Modeguer F., Goulard C., Verbist J.F. 2002. Combined use of LC/MS and a biological test for rapid identification of marine mycotoxins produced by Trichoderma koningii. Journal of Microbiological Methods 48: 181–194. DOI: 10.1016/s0167-7012(01)00322-0.
34.
Leclerc G., Goulard C., Prigent Y., Bodo B., Wroblewski H., Rebuffat S. 2001. Sequences and antimycoplasmic properties of longibrachins LGB II and LGB II, two novel 20-residue peptaibols from Trichoderma longibrachiatum. Journal of Natural Product 64: 164–170.
35.
Li Q.R., Tan P., Yiang Y.L., Hyde K.D., Mckenzie E.H.C., Bahkali A.H., Kang J.C., Wang Y. 2013. A novel Trichoderma species isolated from soil in Guizhou, T. guizhouense. Mycological Progress 12:167–172. DOI: doi.org/10.1007/s11557-012-0821-2.
36.
Lorito M., Farkas V., Rebuffat S., Bodo B., Kubicek C.P. 1996. Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. Journal of Bacteriology 178: 6382–6385. DOI: 10.1128/jb.178.21.6382-6385.1996.
37.
Lorito M., Hayes C.K., di Pietro A., Woo S.L., Harman G.E. 1994. Purification, characterization and synergistic activity of a glucan 1,3-b-glucosidase and an N-acetyl-bglucosaminidase from Trichoderma harzianum. Phytopathology 84: 398–405.
38.
Mouria B., Ouazzani-Touhami A., Douira A. 2008. Effect of various strains of Trichoderma on the growth of a greenhouse tomato crop and their ability to colonize roots and substrate. Phytoprotection 88 (3): 103–110.
39.
Mukherjee P.K., Horwitz B.A., Kenerley C.M. 2012. Secondary metabolism in Trichoderma – a genomic perspective. Microbiology 158: 35–45. DOI: 10.1099/mic.0.053629-0.
40.
Naglot A., Goswami S., Rahman I., Shrimali D.D., Yadav K.K., Gupta V.K., Rabha A.J., Gogoi H.K., Veer V. 2015. Antagonistic potential of native Trichoderma viride strain against potent tea fungal pathogens in north east India. Plant Pathology Journal 31 (3): 278–289. DOI: 10.5423/PPJ.OA.01.2015.0004.
41.
Neuhof T., Dieckmann R., Druzhinina I.S., Kubicek C.P., von Dohren H. 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. DOI: 10.1099/mic.0.2007/006692-0.
42.
Ommati F., Zaker M. 2012. Evaluation of some Trichoderma isolates for biological control of potato wilt disease (Fusarium oxysporum) under lab. and green house conditions. Journal of Crop Protection 1: 279–286.
43.
Panizel I., Yarden O., Ilan M., Carmeli S. 2013. Eight new peptaibols from sponge-associated Trichoderma atroviride. Marine Drugs 11: 4937–4960. DOI: 10.3390/md11124937.
44.
Reino J.L., Guerrero R.F., Hermandez-Galan R., Collado I.G. 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochemistry 7: 89–123. DOI: doi.org/10.1007/s11101-006-9032-2.
45.
Ren J., Xue C., Tian L., Xu M., Chen J., Deng Z., Proksch P., Lin W. 2009. Asperelines A-F, Peptaibols from the Marine-Derived Fungus Trichoderma asperellum. Journal of Natural Product 72: 1036–1044. DOI: 10.1021/np900190w.
46.
Reusser F. 1967. Biosynthesis of antibiotic U-22, 324, a cyclic polypeptide. Journal of Biological Chemistry 242: 243–247.
47.
Röhrich C.R., Iversen A., Jaklitsch W.M., Voglmayr H., Berg A., Dörfelt H., Thrane U., Vilcinskas A., Nielsen K.F., von Döhren H., Brückner H., Degenkolb T. 2012. Hypopulvins, novel peptaibiotics from the polyporicolous fungus Hypocrea pulvinata, are produced during infection of its natural hosts. Fungal Biology 116: 1219–1231. DOI: 10.1016/j.funbio.2012.10.003.
48.
Röhrich C.R., Iversen A., Jaklitsch W.M., Voglmayr H., Vilcinskas A., Nielsen K.F., Thrane U., von Döhren H., Brückner H., Degenkolb T. 2013a. Screening the biosphere: the fungicolous fungus Trichoderma phellinicola, a prolific source of hypophellins, new 17-, 18-, 19-, and 20-residue peptaibiotics. Chemistry Biodiversity 10: 787–812. DOI: 10.1002/cbdv.201200339.
49.
Röhrich C.R., Vilcinskas A., Brückner H., Degenkolb T. 2013b. The sequences of the eleven-residue peptaibiotics: suzukacillins-B. Chemistry Biodiversity 10: 827–837. DOI: 10.1002/cbdv.201200384.
50.
Sivasithamparam K., Ghisalberti E.L. 1998. Secondary metabolism in Trichoderma and Gliocladium. p. 139–191. In: “Trichoderma and Gliocladium” (Harman G.E. and Kubicek C.P., eds.). Vol. 1. London, Taylor and Francis Ltd, UK.
51.
Sriram S., Savitha M.J., Rohini H.S., Jalali S.K. 2013. The most widely used fungal antagonist for plant disease management in India, Trichoderma viride is Trichoderma asperellum as confirmed by oligonucleotide barcode and morphological characters. Current Science 104: 1332–1340.
52.
Stoppacher N., Neumann N.K., Burgstaller L., Zeilinger S., Degenkolb T., Brückner H., Schuhmacher R. 2013. The comprehensive peptaibiotics database. Chemistry Biodiversity 10: 734–743. DOI: 10.1002/cbdv.201200427.
53.
Stoppacher N., Zeilinger S., Omann M., Lassahn P.G., Roitinger A., Krska R., Schuhmacher R. 2008. Characterisation of the peptaibiome of the biocontrol fungus Trichoderma atroviride by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 22: 1889–1898. DOI: 10.1002/rcm.3568.
54.
Vinale F., Sivasithamparam K., Ghisalberti E., Woo S.L., Nigro M., Marra R., Lombardi N., Pascale A., Ruocco M., Lanzuise S., Manganiello G., Lorito M. 2014. Trichoderma secondary metabolites actives on plants and fungal pathogens. The Open Mycology Journal 8: 127–139. DOI: DOI: 10.2174/1874437001408010127.
55.
Vinale F., Marra R., Scala F., Ghisalberti E.L., Lorito M., Sivasithamparam K. 2006. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Letters in Applied Microbiology 43: 143–148. DOI: 10.1111/j.1472-765X.2006.01939.x.
56.
Yabuki T., Miyazaki K., Okuda T. 2014. Japanese species of the Longibrachiatum clade of Trichoderma. Mycoscience 55: 196–212. DOI: 10.1016/J.MYC.2013.08.006.
57.
Yamaguchi K., Tsurumi Y., Suzuki R., Chuaseeharonnachai C., Sri-Indrasutdhi V., Boonyuen N., Okane I., Suzuki K.I., Nakagiri A. 2012. Trichoderma matsushimae and T. aeroaquaticum: two aeroaquatic species with Pseudaegerita-like propagules. Mycologia 104: 1109–1120. DOI: 10.3852/11-253.
58.
Yun B.S., Yoo I.D., Kim Y.S., Lee S.J., Kim K.S., Yeo W.H. 2000. Peptaivirins A and B, two new antiviral peptaibols against TMV infection. Tetrahedron Lett 41: 1429–1431. DOI: doi.org/10.1016/S0040-4039(99)02308-4.