ORIGINAL ARTICLE
Antifungal activity of Trichoderma VOCs against Pyrenophora teres, the causal agent of barley net blotch
| 1 | Centro de Investigaciones de Fitopatología (CIDEFI-CICBA)., Facultad de Ciencias Agrarias y Forestales. Universidad Nacional de La Plata. Calle 60 y 119 s/n, 1900, La Plata, Buenos Aires, Argentina |
| 2 | Instituto de Investigaciones Bioquímicas de La Plata (INIBIOLP-CONICET)., Facultad de Ciencias Médicas, Universidad Nacional de La Plata, 1900, La Plata, Buenos Aires, Argentina |
| 3 | Centro de Investigaciones de Fitopatología (CIDEFI-CICBA),, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata. 1900, La Plata, Buenos Aires, Argentina. |
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
CORRESPONDING AUTHOR
Andrea Vanesa Toledo
Centro de Investigaciones de Fitopatología (CIDEFI-CICBA),, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata. 1900, La Plata, Buenos Aires, Argentina., Avda. 60 y 119 s/n, 1900 La Plata, Argentina
Centro de Investigaciones de Fitopatología (CIDEFI-CICBA),, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata. 1900, La Plata, Buenos Aires, Argentina., Avda. 60 y 119 s/n, 1900 La Plata, Argentina
Submission date: 2017-10-02
Acceptance date: 2017-12-01
Journal of Plant Protection Research 2018;58(1):45–53
KEYWORDS
TOPICS
ABSTRACT
Many species of Trichoderma produce secondary metabolites such as volatile organic compounds (VOCs) that reduce plant diseases and promote their growth. In this work we evaluated the antagonistic effect of VOCs released by eight strains of two Trichoderma species against Pyrenophora teres Drechsler, the causal agent of barley net blotch. Antagonism was estimated based on the percentage of mycelial growth inhibition according to the confronted cultures method. VOCs extraction and identification were performed b y gas chromatography and mass spectrometry, through different methodologies for VOCs emitted by antagonists and pathogens alone or when confronted. VOCs produced by all Trichoderma strains inhibited mycelial growth of the pathogen in a range of 3% to 32%, showing weak and unpigmented mycelia with vacuolization. In addition, P. teres stimulated the release of VOCs by both Trichoderma species. The major groups of VOCs detected were sesquiterpenes, followed by diterpenes, terpenoids and eight-carbon compounds. This is the first report about characterization of volatiles emitted by Trichoderma in presence of P. teres.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (63)
1.
Adams R.P. 2007. Identification of essential oil components by gas chromatography/mass spectrometry. 4th ed. Allured Pub Corp., Carol Stream, IL, USA, 804 pp.
2.
Agüero L.E.M., Alvarado R., Martinez A., Dorta B. 2008. Inhibition of Aspergillus flavus growth and aflatoxin b1 production in stored maize grains exposed to volatile compounds of Trichoderma harzianum Rifai. Interciencia 33 (3): 219–222.
3.
Atanasova L., Le Crom S., Gruber S., Coulpier F., Seidl-Seiboth V., Kubicek C.P., Druzhinina I.S. 2013. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics 14: 121.
4.
Baturo-Ciesniewska A., Grabowski A., Panka D. 2012. Diversity in the Polish isolates of Drechslera teres in spring barley as determined through morphological features, mating types, reaction to control agents and RAPD markers. Journal of Plant Pathology 94 (2): 339–351.
5.
Bell A.A., Wheeler M.H. 1986. Biosynthesis and functions of fungal melanins. Annual Review of Phytopathology 24: 411–451. DOI: https://doi.org/10.1146/annure....
6.
Błaszczyk L., Siwulski M., Sobieralski K., Lisiecka J., Jędryczka M. 2014. Trichoderma spp. – application and prospects for use in organic farming and industry. Journal of Plant Protection Research 54 (4): 309–317. DOI: https://doi.org/10.2478/jppr-2....
7.
Bruce A., Wheatley R.E., Humphris S.N., Hackett C.A., Florence M.E.J. 2000. Production of volatile organic compounds by Trichoderma in media containing different amino acids and their effect on selected wood decay fungi. Holzforschung 54 (5): 481–486. DOI: https://doi.org/10.1515/hf.200....
8.
Butler M.J., Day A.W. 1998. Fungal melanins: a review. Canadian Journal of Microbiology 44 (12): 1115–1136. DOI: https://doi.org/10.1139/w98-11....
9.
Carmona M. 2008. Manual para la identificación y manejo de las enfermedades del cultivo de cebada. Horizonte, Buenos Aires, Argentina, 32 pp.
10.
Calistru C., McLean M., Berjak P. 1997. In vitro studies on the potential for biological control of Aspergillus flavus and Fusarium moniliforme by Trichoderma species. A study of the production of extracellular metabolites by Trichoderma species. Mycopathologia 137: 115–124. DOI: https://doi.org/10.1023/A:1006....
11.
Chiron N., Michelot D. 2005. Odeurs de champignons: chimie et role dans les interactions biotiques- une revue. Cryptogamie Mycologie 26: 299–364.
12.
Citron C.A., Riclea R., Brock N.L., Dickschat J.S. 2011. Biosynthesis of acorane sesquiterpenes by Trichoderma. Journal of Royal Society of Chemistry Advances 1 (2): 290–297. DOI: https://doi.org/10.1039/c1ra00....
13.
Collins R.P., Halim A.F. 1972. Characterization of the major aroma constituent of the fungus Trichoderma viride (Pers.). Journal of Agricultural and Food Chemistry 20 (2): 437–438. DOI: https://doi.org/10.1021/jf6018....
14.
Combet E., Henderson J., Eastwood D.C., Burton K.S. 2006. Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47 (6): 317–326. DOI: https://doi.org/10.1007/s10267....
15.
Contreras-Cornejo H.A., Macías-Rodríguez L., Cortés-Penagos C., López-Bucio J. 2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiology 149 (3): 1579–1592. DOI: https://doi.org/10.1104/pp.108....
16.
Cooney J.M., Lauren D.R., Di Menna M.E. 2001. Impact of competitive fungi on trichothecene production by Fusarium graminearum. Journal of Agricultural and Food Chemistry 49 (1): 522–526. DOI: https://doi.org/10.1007/s12550....
17.
Demain A.L., Fang A. 2000. The natural functions of secondary metabolites. Advances in Biochemical Engineering/Biotechnology 69: 1–39.
18.
Dennis C., Webster J. 1971. Antagonistic properties of species groups of Trichoderma: II. Production of volatile antibiotics Transactions of the British Mycological Society 57 (1): 41–48. DOI: https://doi.org/10.1016/S0007-....
19.
El-Hasan A., Walker F., Buchenauer H. 2008. Trichoderma harzianum and its metabolite 6-pentyl-alphapyrone suppress fusaric acid produced by Fusarium moniliforme. Journal of Phytopathology 156 (2): 79–87. DOI: https://doi.org/10.1111/j.1439....
20.
Hajieghrari B., Torabi-Giglou M., Mohammadi M.R., Davari M. 2008. Biological potential of some Iranian Trichoderma isolates in the control of soil borne plant pathogenic fungi. African Journal of Biotechnology 7 (8): 967–972.
21.
Harman G.E., Howell C.R., Viterbo A., Chet I., Lorito M. 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews in Microbiology 2 (1): 43–56. DOI: https://doi.org/10.1038/nrmicr....
22.
Herrero-Garcia E., Garzia A., Cordobesa S., Espeso E.A., Ugalde U. 2011. 8-Carbon oxylipins inhibit germination and growth, and stimulate aerial conidiation in Aspergillus nidulans. Fungal Biology 115 (4–5): 393–400. DOI: https://doi.org/10.1016/j.funb....
23.
Heydari A., Pessarakli M. 2010. A review on biological control of fungal plant pathogens using microbial antagonists. Journal of Biological Sciences 10 (4): 273–290. DOI: https://doi.org/10.3923/jbs.20....
24.
Hoitink H.A.J., Madden L.V., Dorrance A.E. 2006. Systemic resistance induced by Trichoderma spp.: interactions between the host, the pathogen, the biocontrol agent, and soil organic matter quality. Phytopathology 96 (2): 186–189. DOI: https://doi.org/10.1094/phyto-....
25.
Howell C.R. 1998. The role of antibiosis in biocontrol. p. 173–184. In: “Trichoderma and Gliocladium” (G.E. Harman, C.P. Kubicek, eds.). Taylor and Francis, London, UK.
26.
Hubbell S.P., Wiemer D.F., Adejare A. 1983. An antifungal terpenoid defends a neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia 60 (3): 321–327. DOI: https://doi.org/10.1007/bf0037....
27.
Humphris S.N., Bruce A., Buultjens E., Wheatley R.E. 2002. The effects of volatile microbial secondary metabolites on protein synthesis in Serpula lacrymans. FEMS Microbiology Letters 210 (2): 215–219.
28.
Hung R., Lee S., Bennett J.W. 2015. Fungal volatile organic compounds and their role in ecosystems. Applied Microbiology and Biotechnology 99: 3395–3405. DOI: https://doi.org/10.1007/s00253....
29.
Inoue Y., Shiraishi A., Hada T., Hirose K., Hamashima H., Shimada J. 2004. The antibacterial effects of terpene alcohols on Staphylococcus aureus and their mode of action. FEMS Microbiology Letters 237 (2): 325–331. DOI: https://doi.org/10.1111/j.1574....
30.
Jacobson E.S. 2000. Pathogenic roles for fungal melanins. Clinical Microbiology Reviews 13 (4): 708–717.
31.
Jalali F., Zafari D., Salari H. 2017. Volatile organic compounds of some Trichoderma spp. increase growth and induce salt tolerance in Arabidopsis thaliana. Fungal Ecology 29: 67–75. DOI: http://dx.doi.org/10.1016/j.fu....
32.
Khaledi N., Taheri P. 2016. Biocontrol mechanisms of Trichoderma harzianum against soybean charcoal rot caused by Macrophomina phaseolina. Journal of Plant Protection Research 56 (1): 21–31. DOI: https://doi.org/10.1515/jppr-2....
33.
Kishimoto K., Matsui K., Ozawa R., Takabayashi J. 2007. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. Journal of General Plant Pathology 73 (1): 35–37. DOI: https://doi.org/10.1007/s10327....
34.
Korpi A., Jarnberg J., Pasanen A.L. 2009. Microbial volatile organic compounds. Critical Reviews in Toxicology 39 (2): 139–193. DOI: https://doi.org/10.1080/104084....
35.
Kottb M., Gigolashvili T., Großkinsky D.K., Piechulla B. 2015. Trichoderma volatiles effecting Arabidopsis: from inhibition to protection against phytopathogenic fungi. Frontiers in Microbiology 6: 995. DOI: https://doi.org/10.3389/fmicb.....
36.
Kovats E.S. 1965. Gas chromatographic characterization of organic substances in the retention index system. Advances in Chromatography 1: 229–247.
37.
Kramer R., Abraham W.R. 2012. Volatile sesquiterpenes from fungi: what are they good for? Phytochemistry Reviews 11: 15–37. DOI: https://doi.org/10.1007/s11101....
38.
Lee S., Yap M., Behringer G., Hung R., Bennett J.W. 2016. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biology and Biotechnology 3 (1): 7. DOI: https://doi.org/10.1186/s40694....
39.
Lemfack M.C., Nickel J., Dunkel M., Preissner R., Piechulla B. 2013. VOC: a database of microbial volatiles. Nucleic Acids Research 42: D744–D748. DOI: https://doi.org/10.1093/nar/gk....
41.
Mathys J., De Cremer K., Timmermans P., Van Kerckhove S., Lievens B., Vanhaecke M., Cammue B.P.A., De Coninck B. 2012. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Frontiers in Plant Science 3: 108. DOI: https://doi.org/10.3389/fpls.2....
42.
Michereff S.J., Silveira N.S.S., Reis A., Mariano R.L.R. 1994. Epiphytic bacteria antagonistic to Curvularia leaf spot of yam. Microbial Ecology 28 (1): 101–110.
43.
Minerdi D., Bossi S., Maffei M.E., Gullino M.L., Garibaldi A. 2011. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansion A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiology Ecology 76 (2): 342–351. DOI: https://doi.org/10.1111/j.1574....
44.
Moya P. 2017. Antagonismo y efecto biocontrolador de Trichoderma spp. sobre Drechslera teres, agente causal de la “mancha en red” de la cebada (Hordeum vulgare L. var. vulgare). SEDICI Repositorio Institucional de la UNLP. Available on: http://sedici.unlp.edu.ar/hand....
45.
Mukherjee P.K., Horwitz B.A., Singh U.S., Mukherjee M., Schmoll M. 2013. Trichoderma in agriculture, industry and medicine: an overview. p. 1–9. In: “Trichoderma biology and applications” (P.K. Mukherjee, B.A. Horwitz, U.S. Singh, M. Mukherjee, M. Schmoll, eds.). CAB International, Boston, USA, 327 pp.
46.
Nemčovič M., Jakubíková L., Víden I., Farkaš V. 2008. Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiology Letters 284 (2): 231–236. DOI: https://doi.org/10.1111/j.1574....
47.
Nieto-Jacobo M.F., Steyaert J.M., Salazar-Badillo F.B., Nguyen D.V., Rostás M., Braithwaite M., De Souza J.T., Jimenez-Bremont J.F., Ohkura M., Stewart A., Mendoza-Mendoza A. 2017. Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Frontiers in Plant Science 8: 102. DOI: https://doi.org/10.3389/fpls.2....
48.
Polizzi V., Adams A., Picco A.M., Adriaens E., Lenoir J., Van Peteghem C., De Saeger S., De Kimpe N. 2011. Influence of environmental conditions on production of volatiles by Trichoderma atroviride in relation with the sick building syndrome. Building and Environment 46 (4): 945–954. DOI: https://doi.org/10.1016/j.buil....
49.
Reino J.L., Guerrero R.F., Hernández-Galán R., Collado I.G. 2008. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochemistry Reviews 7 (1): 89–123. DOI: https://doi.org/10.1007/s11101....
50.
Sánchez A.D., Barrera V., Reybet G.E., Sosa M.C. 2015. Biocontrol con Trichoderma spp. de Fusarium oxysporum causal del “mal de almácigos” en pre y post emergencia en cebolla. Revista de la Facultad de Agronomía, La Plata 114 (1): 61–70.
51.
Schenkel D., Lemfack M.C., Piechulla B., Splivallo R. 2015. A meta-analysis approach for assessing the diversity and specificity of belowground root and microbial volatiles. Frontiers in Plant Science 6: 707. DOI: https://doi.org/10.3389/fpls.2....
52.
Schuster A., Schmoll M. 2010. Biology and biotechnology of Trichoderma. Applied Microbiology and Biotechnology 87 (3): 787–799. DOI: https://doi.org/10.1007/s00253....
53.
Shahiri Tabarestani M., Rahnama K., Jahanshahi M., Nasrollahnejad S., Fatemi M.H. 2016. Identification of volatile organic compounds of Trichoderma spp. using static headspace gas chromatography-mass spectrometry. Mycologia Iranica 3 (1): 47–55. DOI: https://doi.org/10.22043/mi.20....
54.
Siddiquee S., Cheong B.E., Taslima K., Kausar H., Hasan M.M. 2012. Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. Journal of Chromatographic Science 50: 358–367. DOI: https://doi.org/10.1093/chroms....
55.
Stoppacher N., Kluger B., Zeilinger S., Krska R., Schuhmacher R. 2010. Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPMEGC-MS. Journal of Microbiological Methods 81: 187–193. DOI: https://doi.org/10.1016/j.mime....
56.
Szabó M., Csepregi K., Gálber M., Virányi F., Fekete C. 2012. Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: The role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biological Control 63 (2): 121–128. DOI: https://doi.org/10.1016/j.bioc....
57.
Tekauz A., Mills J.T. 1974. New types of virulence in Pyrenophora teres in Canada. Canadian Journal of Plant Science 54 (4): 731–734. DOI: https://doi.org/10.4141/cjps74....
58.
Verma M., Brar S., Tyagi R., Surampalli R., Valero J. 2007. Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochemical Engineering Journal 37 (1): 1–20. DOI: https://doi.org/10.1016/j.bej.....
59.
Vinale F., Sivasithamparam K., Ghisalberti E.L., Marra R., Barbetti M.J., Li H., Woo S.L., Lorito M. 2008. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiological and Molecular Plant Pathology 72: 80–86. DOI: https://doi.org/10.1016/j.pmpp....
60.
Vos C.M.F., DeCremer K., Cammue B.P.A., DeConinck B. 2015. The toolbox of Trichoderma spp. in biocontrol of Botrytis cinerea disease. Molecular Plant Pathology 16 (4): 400–412. DOI: https://doi.org/10.1111/mpp.12....
61.
Wheatley R.E. 2002. The consequences of volatile organic compound mediated bacterial and fungal interactions. Antonie van Leeuwenhoek 81 (1-4): 357–364.
62.
Zeilinger S., Schuhmacher R. 2013. Volatile organic metabolites of Trichoderma spp.: Biosynthesis, biology and analytics. p. 10–42. In: “Trichoderma Biology and Applications” (P.K. Mukherjee, B.A. Horwitz, U.S. Singh, M. Mukherjee, M. Schmoll, eds.). CAB International, Boston, USA.
63.
Zhang F., Yang X., Ran W., Shen Q. 2014. Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum T-E5. FEMS Microbiology Letters 359: 116–123. DOI: https://doi.org/10.1023/A:1020....
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