ORIGINAL ARTICLE
Combinations of Tagetes filifolia Lag. essential oil with chemical fungicides to control Colletotrichum truncatum and their effects on the biocontrol agent Trichoderma harzianum
More details
Hide details
1
Estacioń Experimental Agropecuaria Marcos Juárez/Laboratorio de Fitopatologia, Instituto Nacional de Tecnología Agropecuaria
(INTA), Córdoba, Argentina
2
Microbiologia Agricola, Facultad de Ciencias Agropecuarias-Universidad nacional de Cordoba (UNC), Córdoba, Argentina
3
Instituto Multidisciplinario de Biología Vegetal (IMBIV), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, 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
Submission date: 2019-06-17
Acceptance date: 2019-08-07
Online publication date: 2020-03-06
Corresponding author
Boris Xavier Camiletti
Microbiologia Agricola, Facultad de Ciencias Agropecuarias-Universidad nacional de Cordoba (UNC), Feliz Marrone 746, X5000, Cordoba, Argentina
Journal of Plant Protection Research 2020;60(1):41-50
KEYWORDS
TOPICS
ABSTRACT
Soybean [Glycine max (L.)], one of the most important crops in Argentina, is commonly
infected by Colletotrichum truncatum, the causal agent of anthracnose. Tagetes filifolia essential
oil (EO) is presented as a natural approach to minimize the dose of chemical fungicides
applied to the crop. The fungus Trichoderma harzianum is used as a biocontrol
agent because of its ability to produce secondary metabolites that destroy cell walls of phytopathogenic
fungi. However, its performance can be affected when it is exposed to chemical
fungicides. The objective of this work was to evaluate the antifungal activity of T. filifolia
EO both individually and combined with chemical fungicides against C. truncatum, and its
effect on T. harzianum. Fungi were isolated from soybean crops. The following pesticides
were assessed: carbendazim (F1), difenoconazole (F2) and trifloxystrobin + cyproconazole
(F3). The EO was obtained from native plants and its chemical composition was analyzed
by gas chromatography–mass spectrometry (GC–MS). The minimum fungicide concentration
(MFC) was determined for each compound. Fungicides were combined with the EO
to look for combinations that allowed a reduction of pesticide doses. Among fungicides,
F1 showed the strongest antifungal activity against C. truncatum (MFC = 0.25 μl ⋅ l–1) and
T. harzianum (MFC = 1.5 μl ⋅ l–1). The sensitivity of both fungi to the EO was lower than
to fungicides. The EO presented MFCs of 6,000 and 9,000 μl ⋅ l–1 against C. truncatum and
T. harzianum. The EO and F1 affected the growth of T. harzianum at concentrations that
controlled C. truncatum (31 and 10%). Eight combinations of fungicides and the EO allowed
fungicide concentration reductions of up to 80%, although the growth of the biocontrol
strain was also affected. The results demonstrated that T. filifolia EO can be used to control
anthracnose and reduce doses of chemical fungicides applied to soybean crops. Its effect on
T. harzianum should be considered in the design of integrated pest management strategies.
ACKNOWLEDGEMENTS
The authors wish to thank the National Institute of
Agricultural Technology (INTA), National University
of Cordoba, Secretary of Science and Technology
(UNC, SECyT) and the Argentinian National Research
Council (CONICET) for their financial support. We
are also grateful to the College of Agricultural Science
(FCA-UNC) for allowing us to use its laboratory
equipment.
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (66)
1.
Abbaszadeh S., Sharifzadeh A., Shokri H., Khosravi A.R., Abbaszadeh A. 2014. Antifungal efficacy of thymol, carvacrol, eugenol and menthol as alternative agents to control the growth of food-relevant fungi. Journal of Mycologie Medicale 24 (2): e51–e56. DOI:
https://doi.org/10.1016/j.mycm....
2.
Abdel-Kader M., El-Mougy N., Lashin S. 2011. Essential oils and Trichoderma Harzianum as an integrated control measure against faba bean root rot pathogens. Journal of Plant Protection Research 51 (3): 306–313. DOI:
https://doi.org/10.2478/v10045....
3.
Abrol D.P., Shankar U. 2016. Integrated Pest Management. p. 523–549. In: “Breeding Oilseed Crops for Sustainable Production” (S.K. Gupta, ed.). Elsevier Inc. Netherlands, 994 pp.
4.
Adams R.P. 1995. Identification of Essential Oils by Ion Trap Mass Spectroscopy. Carol Stream, IL, USA, Allured Publishing, 843 pp.
5.
Amber K., Aijaz A., Immaculata X., Luqman K.A., Nikhat M. 2010. Anticandidal effect of Ocimum sanctum essential oil and its synergy with fluconazole and ketoconazole. Phytomedicine 17: 921–925. DOI: 10.1016/j.phymed.2010.02.012.
6.
Angelini P., Pagiotti R., Granetti B. 2008. Effect of antimicrobial activity of Melaleuca alternifolia essential oil on antagonistic potential of Pleurotus species against Trichoderma harzianum in dual culture. World Journal of Microbiology and Biotechnology 24: 197–202. DOI: 10.1007/s11274-007-9456-x.
7.
Armostrong-Cho C.L., Banniza S. 2006. Glomerella truncata sp. nov., the teleomorph of Colletotrichum truncatum. Mycological Research 110 (8): 951–956. DOI:
https://doi.org/10.1016/j.mycr....
8.
Arrebola E., Sivakumar D., Bacigalupo R., Korsten L. 2010. Combined application of antagonist Bacillus amyloliquefaciens and essential oils for the control of peach postharvest diseases. Crop Protection 29 (4): 369–377. DOI:
https://doi.org/10.1016/j.crop....
9.
Asensio C.M., Nepote V., Grosso N.R. 2011. Chemical stability of extra-virgin olive oil added with oregano essential oil. Journal of Food Science 76: 445–450. DOI:10.1111/j.1750-3841.2011.02332.x.
10.
Bakkali F., Averbeck S., Averbeck D., Idaomar M. 2008. Biological effects of essential oils – a review. Food Chemical Toxicology 46: 446–75. DOI: 10.1016/j.fct.2007.09.106.
11.
Benítez T., Rincón A.M., Limón M.C., Codón A.C. 2004. Biocontrol mechanisms of Trichoderma strains. International Microbiology 7: 249–260.
12.
Bluma R., Amaiden M.R., Daghero J., Etcheverry M. 2008. Control of Aspergillus section Flavi growth and aflatoxin accumulation by plant essential oils. Journal of Applied Microbiology 105 (1): 203–214. DOI:
https://doi.org/10.1111/j.1365....
13.
Camiletti B.X. 2018. Estrategias de manejo de Aspergillus flavus y Penicillium spp. para la reducción de los niveles de micotoxinas en maíz. Ph.D. Thesis, Universidad Nacional de Cordoba, Spain.
14.
Camiletti B.X., Asensio C.M., Gadban L.C., Pecci M. de la P.G., Conles M.Y., Lucini E.I. 2016. Essential oils and their combinations with iprodione fungicide as potential antifungal agents against withe rot (Sclerotium cepivorum Berk) in garlic (Allium sativum L.) crops. Industrial Crops and Products 85: 117–124. DOI:
https://doi.org/10.1016/j.indc....
15.
Camiletti B.X., Asensio C.M., Pecci M.D.L.P.G., Lucini E.I. 2014. Natural control of corn postharvest fungi Aspergillus flavus and Penicillium spp. using essential oils from plants grown in Argentina. Journal of Food Science 79 (12): M2499–M2506. DOI:
https://doi.org/10.1111/1750-3....
16.
Carmona M., Gally M., Sautua F., Abello A., Lopez P. 2011. Uso de mezclas de azoxistrobina y triazoles para controlar enfermedades de fin de ciclo de la soja. [Use of azoxystrobin and triazoles mixtures to control late season diseases in soybean crop]. Summa Phytopatholica 37 (2): 134–139. DOI:
https://doi.org/10.1590/s0100-... (in Spanish with English abstract).
17.
Carmona M., Sautua F., Perelman S., Gally M., Reis E.M. 2015. Development and validation of a fungicide scoring system for management of late season soybean diseases in Argentina. Crop Protection 70: 83–91. DOI: 10.1016/j.cropro.2015.01.019.
18.
Chen S.N., Luo C.X., Hu M.J., Schnabel G. 2016. Sensitivity of Colletotrichum species, including C. fioriniae and C. nymphaeae, from peach to demethylation inhibitor fungicides. Plant Disease 100: 2434–2441. DOI: 10.1094/PDIS-04-16-0574-RE.
19.
Dhingra O.D., Sinclair J.B. 1995. Basic Plant Pathology Methods. CRC Press, Florida, United States, 444 pp.
20.
Dias M.D., Pinheiro V.F., Café-filho A.C. 2016. Impact of anthracnose on the yield of soybean subjected to chemical control in the north region of Brazil. Summa Phythopathologica 42 (1): 18–23. DOI:
https://doi.org/10.1590/0100-5....
22.
De Feo V., Della Porta G., Urrunaga Soria E., Urrunaga Soria R., Senatore F. 1998. Composition of the essential oil of Tagetes filifolia Lag. Flavour Fragrance Journal 13: 145–147. DOI: 10.1002/(SICI)1099-1026(199805/06).
23.
Fernandez-Ortuño D., Chen F., Schnabel G. 2012. Resistance to pyraclostrobin and boscalid in Botrytis cinerea isolates from strawberry fields in the Carolinas. Plant Disease 96 (8): 1198–1203. DOI:
https://doi.org/10.1094/pdis-1....
24.
Ganuza M., Pastor N., Erazo J., Andrés J., Reynoso M.M., Rovera M., Torres A.M. 2017. Efficacy ofthe biocontrol agent Trichoderma harzianum ITEM 3636 against peanut smut, an emergent disease caused by Thecaphora frezii. European Journal of Plant Pathology 151 (1): 257–262. DOI:
https://doi.org/10.1007/s10658....
25.
Gawade D., Phule M., Vidyapeeth K., Gawade D. 2009. Field evaluation of fungicides, botanicals and bioagents against anthracnose of soybean. Agricultural Science 29: 174–177.
26.
Gisi U. 1991. Sinergism between fungicides for control of Phytophthora. p. 361–372. In: “Phytophthora” (J.A. Lucas, D.S. Shattock, L.R. Cooke, eds.). Cambridge University Press, Cambridge, UK, 1089 pp.
27.
Gisi U. 1996. Synergistic interactions of fungicides in mixtures. Phytopathology 86: 1273–1279.
28.
Gisi U., Binde H., Rimbach E. 1985. Synergistic interactions of fungicides with different modes of action. Transactions of the British Mycological Society 85: 299–306. DOI: 10.1016/S0007-1536(85)80192-3.
29.
Goncalves S.S., Souza A.C.R., Chowdhary A., Meis J.F., Colombo A.C. 2016. Epidemiology and molecular mechanisms of antifungal resistance in Candida and Aspergillus. Mycoses 59: 198–219. DOI: 10.1111/myc.12469.
30.
Grondona I., Hermosa R., Tejada M., Gomis M.D., Mateos P.F., Bridge P.D. 1997. Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soilborne fungal plant pathogens. Applied Environmental Microbiology 63: 3189–3198. DOI: 0099-2240/97/$04.0010.
31.
Huang Y., Zhao J., Zhou L., Wang J., Gong Y., Chen X. 2010. Antifungal activity of the essential oil of Illicium verum fruit and its main component trans-anethole. Molecules 15: 7558–7569. DOI: 10.3390/molecules15117558.
33.
Karapinar M. 1990. Inhibitory effects of anethole and eugenol on the growth and toxin production of Aspergillus parasiticus. International Journal of Food Microbiology 10: 193–199. DOI: 10.1016/0168-1605(90)90066-E.
34.
Kosman E., Cohen Y. 1996. Procedures for calculating and differenciating synergism and antagonim in action of fungicide mixtures. Phytopathology 86: 1263–1272.
35.
Lim S., Shin S. 2008. Combined effects of the essential oil from Eucalyptus globulus with ketoconazole against Candida and Trichophyton species. Natural Products Science 14 (1): 1–12.
36.
Lucini E.I. 2004. Cambios en la composición lipídica del micelio de Sclerotinia sclerotiorum (Lib.) de Bary y Sclerotium cepivorum Berk por acción de terpenos. Ph.D. Thesis. Universidad Nacional de Cordoba, Spain.
37.
Lucini E.I., Zunino M.P., Lopez M.L., Zygadlo J.A. 2006. Effect of monoterpenes on lipid composition and sclerotial development of Sclerotium cepivorum Berk. Journal of Phytopathology 154 (7–8): 441–446. DOI:
https://doi.org/10.1111/j.1439....
38.
Maestri D.M., Zygadlo J.A., Grosso N.R., Aburrá R.E. 1991. Composición del aceite esencial en poblaciones de Tagetes filifolia. Annals of Biology 17: 133–136.
39.
Magi G., Marini E., Facinelli B. 2015. Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin against clinical erythromycin-resistant Group A Streptococci. Frontiers in Microbiology 6: 1–7. DOI:
https://doi.org/10.3389/fmicb.....
40.
Manandhar J.B., Hartman G.L. 1999. Anthracnose. p. 13–14. In: “Compendium of Soybean Disease” (G.L. Hartman, J.B. Sinclair, J.C Rupe, eds.). American Phytopathological Society, St. Paul, MN, 238 pp.
41.
Marei G.I.K., Abdel Rasoul M.A., Abdelgaleil S.A.M. 2012. Comparative antifungal activities and biochemical effects of monoterpenes on plant pathogenic fungi. Pesticide Biochemestry and Physiology 103 (1): 56–61. DOI:
https://doi.org/10.1016/j.pest....
42.
Marotti M., Piccaglia R., Biavati B., Marotti I., Marotti M., Piccaglia R. 2011. Characterization and yield evaluation of essential oils from different tagetes species. Journal of Essential Oil Research 15: 37–41. DOI:
https://doi.org/10.1080/104129....
43.
Nikkhah M., Hashemi M., Habibi Najafi M.B., Farhoosh R. 2017. Synergistic effects of some essential oils against fungal spoilage on pear fruit. International Journal of Food Microbiology 257: 285–294. DOI:
https://doi.org/10.1016/j.ijfo....
44.
Odds F.C. 2003. Synergy, antagonism, and what the chequerboard puts between them. Journal of Antimicrobial Chemotherapy 52 (1): 1. DOI:
https://doi.org/10.1093/jac/dk....
45.
Oh J.H., Kang N.W. 2002. Efficacy of fluazinam and Iprodione + Propineb in the supression of Diaporthe phaseolorum, Colletotrichum truncatum and Cercospora kikuchii, the causal agents of seed decay in soybean. Plant Pathology Journal 18 (4): 216–220. DOI:
https://doi.org/10.5423/ppj.20....
46.
Omidbeygi M., Barzegar M., Hamidi Z., Naghdibadi H. 2007. Antifungal activity of thyme, summer savory and clove essential oils against Aspergillus flavus in liquid medium and tomato paste. Food Control 18 (12): 1518–1523. DOI:
https://doi.org/10.1016/j.food....
47.
Pavela R. 2014. Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) larvae. Industrial Crops and Products 60: 247–258. DOI:
https://doi.org/10.1016/j.indc....
48.
Phélinas P., Choumert J. 2017. Is GM soybean cultivation in Argentina sustainable? World Development 99: 452–462. DOI: 10.1016/j.worlddev.2017.05.033.
49.
Pillai S.K., Moellering R.C., Eliopoulos G.M. 2005. Antimicrobial combinations. p. 365–340. In: “Antibiotics in Laboratory Medicine” (V. Lorian, ed.). Lippincott, Williams and Wilkin, Philadelphia, USA, 1099 pp.
50.
Plodpai P., Chuenchitt S., Petcharat V., Chakthong S., Voravuthikunchai S.P. 2013. Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Protection 43: 65–71. DOI: 10.1016/j.cropro.2012.09.004.
51.
Pyun M.S., Shin S. 2006. Antifungal effects of the volatile oils from Allium plants against Trichophyton species and synergism of the oils with ketoconazole. Phytomedicine 13 (6): 394–400. DOI:
https://doi.org/10.1016/j.phym....
52.
Ramos A.M., Tadic F.L., Cinto I., Carmona M., Gally M. 2013. Molecular characterization of Colletotrichum species causing soybean anthracnose in Argentina. Mycotaxon 123 (1): 457–465.
53.
Rampersad S.N., Teelucksingh L.D., Indies W., Sciences L., Science F. 2012. Differential responses of Colletotrichum gloeosporioides and C. truncatum isolates from different hosts to multiple fungicides based on two assays. Plant Disease 96 (10): 1526–1536. DOI:
https://doi.org/10.1094/pdis-1....
54.
Rifai M.A. 1969. A revision of the genus Trichoderma. Mycological Papers 116: 1–56.
55.
Sarkar S., Narayanan P., Divakaran A., Balamurugan A., Premkumar R. 2010. The in vitro effect of certain fungicides, insecticides, and biopesticides on mycelial growth in the biocontrol fungus Trichoderma harzianum. Turkish Journal Biology 34: 399–403. DOI: 10.3906/biy-0812-4.
56.
Serrato Cruz M.A., Reyes Trejo B., Ortega Arenas L., Domingo Gómez A., Gómez Sánchez N., López Martínez F. 2003. Anisillo (Tagetes filifolia Lag.): Recurso genético mexicano para controlar la mosquita blanca (Bemicia sp. y Trialurodes sp.). Revista del Jardín Botánico Nacional 24: 65–70.
57.
Sharma V., Salwan R., Sharma P.N., Kanwar S.S. 2017. Elucidation of biocontrol mechanisms of Trichoderma harzianum against different plant fungal pathogens: Universal yet host specific response. International Journal of Biological Macromolecules 95: 72–79. DOI:
https://doi.org/10.1016/jijbio....
58.
Shin S., Kang C.A. 2003. Antifungal activity of the essential oil of Agastache rugosa Kuntze and its synergism with ketoconazole. Letters in Applied Microbiology 36 (2): 111–115. DOI:
https://doi.org/10.1046/j.1472....
59.
Sosa-Gomez D.R., Delpin K.E., Moscardi F., Nozaki M. 2003. The impact of fungicides on Nomurea rileyi (Farlow) Samson epizootics and populations of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), on soybean. Neotropical Entomology 32 (2): 287–291. DOI:
https://doi.org/10.1590/s1519-....
60.
Sushir M.A., Suryawanshi K.K., Patole S.P. 2015. Sensitivity of Trichoderma harzianum Rifai against systemic fungicides. International Journal of Applied Research 1: 403–405.
61.
Szkolnik M. 1981. Physical modes of action of sterol-inhibiting fungicides against apple diseases Venturia inaequalis. Plant Disease 65 (12): 981–985. DOI:
https://doi.org/10.1094/pd-65-....
62.
Thompson D.G., Kreutrweiser D.P. 2007. A review of the environmental fate and effects of natural “reduced-risk” pesticides in Canada. ACS Symposium 947: 245–274.
63.
Torres-Calzada C., Tapia-Tussell R., Higuera-Ciapara I., Martin-Mex R., Nexticapan-Garcez A., Perez-Brito D. 2015. Sensitivity of Colletotrichum truncatum to four fungicides and characterization of thiabendazole-resistant isolates. Plant Disease 99 (11): 1590–1595. DOI:
https://doi.org/10.1094/pdis-1....
64.
Vollmann J. 2016. Soybean versus other food grain legumes: A critical appraisal of the United Nations International Year of Pulses 2016. Journal of Land Management, Food Environment 67: 17–24. DOI: 10.1515/boku-2016-0002.
65.
Zavala León M.J., Tun Suárez J.M., Cristóbal Alejo J., Ruiz Sánchez E., Gutierrez Alonso O., Vázquez Calderón M. 2005. Control postcosecha de la antracnosis en papaya y sensibilidad de Colletotrichum gloeosporioides (Penz.) Sacc. a fungicidas organosintéticos. Revista Chapingo – Serie Horticultura 11: 251–255.
66.
Zygadlo J., Guzman C.A., Grosso N.R. 1994. Antifungal properties of the leaf oils of Tagetes minuta L. and Tagetes filifolia Lag. Journal of Essential Oil Research 6: 617–621. DOI: 10.1080/10412905.1994.9699353.