Published

2023-12-31

Characterization of Trichoderma species from agricultural soils of Paraguay

Caracterización de especies de Trichoderma de suelos agrícolas de Paraguay

DOI:

https://doi.org/10.15446/agron.colomb.v41n3.111299

Keywords:

biological control, phylogenetics, fungi, taxonomy (en)
control biológico, filogenética, hongos, taxonomía (es)

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Authors

  • Andrés Dejesús Sanabria-Velázquez North Carolina State University - Department of Entomology and Plant Pathology - Raleigh, NC - USA https://orcid.org/0000-0002-2038-5388
  • Marcos Marcelo Florentín Pavía Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Biotecnología - San Lorenzo, Paraguay https://orcid.org/0000-0002-5969-468X
  • Lorena Insaurralde Ayala Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Biotecnología - San Lorenzo, Paraguay
  • María Eugenia Flores-Giubi Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Química Biológica - San Lorenzo, Paraguay https://orcid.org/0000-0002-1572-9983
  • María Cristina Romero-Rodríguez Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Química Biológica - San Lorenzo, Paraguay https://orcid.org/0000-0003-3979-0348
  • Pablo Hernán Sotelo Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Biotecnología - San Lorenzo, Paraguay https://orcid.org/0000-0002-6473-2134
  • Javier E. Barúa Universidad Nacional de Asunción - Facultad de Ciencias Químicas - Departamento de Química Biológica - San Lorenzo, Paraguay https://orcid.org/0000-0002-8164-3432

There is a growing interest in the development of sustainable alternatives to the use of chemical pesticides for pest management in agricultural systems. This research aimed to isolate and characterize native strains of Trichoderma spp. from different soils of Paraguay using morphological and molecular criteria. We processed plant and soil samples from eight commercial farms distributed in different departments of Paraguay and isolated 14 monosporic isolates of Trichoderma spp., obtaining two isolates from the Department of Alto Paraná (FCQ36 and FCQ37), four isolates from Cordillera (FCQ42, FCQ43, FCQ44, and FCQ46), one isolate from Central (FCQ32), and seven isolates from Itapúa (FCQ13, FCQ16, FCQ18, FCQ19, FCQ21, FCQ23, and FCQ47). In addition, phylogenetic analyses using the ITS and tef1α loci were carried out. A better resolution of the tef1a gene than the ITS region was observed. Moreover, a third phylogenetic tree from the concatenated ITS and tef1α sequences matrix was generated, obtaining the same topology with higher bootstrap support values. Through this approach, we reported for the first time the presence of Trichoderma koningiopsis (FCQ19, FCQ36, and FCQ37), Trichoderma neokoningii (FCQ13), and Trichoderma asperellum (FCQ42, FCQ43, FCQ44, and FCQ46), Trichoderma brevicompactum (FCQ18 and FCQ21), and Trichoderma longibrachiatum (FCQ 47) in Paraguay. The Trichoderma species identified in this study can be used to develop effective biocontrol products for agricultural and industrial purposes in Paraguay.

Existe un creciente interés en el desarrollo de alternativas sostenibles al uso de plaguicidas químicos para el manejo de plagas en los sistemas agrícolas. El objetivo de este trabajo fue aislar y caracterizar por criterios morfológicos y moleculares cepas nativas de Trichoderma spp. de diferentes suelos de Paraguay. Se procesaron muestras de plantas y suelo de ocho fincas comerciales distribuidas en diferentes departamentos de Paraguay para el aislamiento de 14 aislados monospóricos de Trichoderma spp., obteniendo dos aislados del Departamento de Alto Paraná (FCQ36 y FCQ37), cuatro aislados de Cordillera (FCQ42, FCQ43, FCQ44 y FCQ46), un aislado de Central (FCQ32) y siete aislados de Itapúa (FCQ13, FCQ16, FCQ18, FCQ19, FCQ21, FCQ23 y FCQ47). Además, se realizaron análisis filogenéticos utilizando los loci ITS y tef1α. Se observó una mejor resolución del gen tef1α en comparación con la región ITS. Además, se generó un tercer árbol filogenético a partir de la matriz concatenada de ambas secuencias ITS y tef1α obteniendo la misma topología con mayores valores de soporte bootstrap. A través de este enfoque, se reporta por primera vez la presencia de Trichoderma koningiopsis (FCQ19, FCQ36 y FCQ37), Trichoderma neokoningii (FCQ13) y Trichoderma asperellum (FCQ42, FCQ43, FCQ44 y FCQ46), Trichoderma brevicompactum (FCQ18 y FCQ21) y Trichoderma longibrachiatum (FCQ47) en Paraguay. Las especies de Trichoderma identificadas en este trabajo pueden ser utilizadas en el desarrollo de productos de control biológico eficaces para fines agrícolas e industriales en Paraguay.

References

Akagi, T., Kawamura, C., Terasawa, N., Yamaguchi, K., & Kubo, K. (2017). Suspected pulmonary infection with Trichoderma longibrachiatum after allogeneic stem cell transplantation. Internal Medicine, 56(2), 215–219. https://doi.org/10.2169/internalmedicine.56.5316 DOI: https://doi.org/10.2169/internalmedicine.56.5316

Albrecht, A. B., Albrecht, M., & Morinigo, K. (2017). Determinación de Trichoderma sp. en raíz del cultivo de chía (Salvia hispánica L). Agrotecnia, 25, 13–13. https://doi.org/10.30972/agr.0252445 DOI: https://doi.org/10.30972/agr.0252445

Alkooranee, J. T., & Kadhum, N. N. (2019). Induce systemic resistance in cucumber by some bio-elicitors against Alternaria leaf blight disease caused by Alternaria cucumerina fungus. Plant Archives, 19(1), 747-755. https://www.plantarchives.org/PDF%2019-1/747-755%20(4656).pdf

Altintas, S., & Bal, U. (2008). Effects of the commercial product based on Trichoderma harzianum on plant, bulb and yield characteristics of onion. Scientia Horticulturae, 116(2), 219–222. https://doi.org/10.1016/j.scienta.2007.11.012 DOI: https://doi.org/10.1016/j.scienta.2007.11.012

Amerio, N. S., Castrillo, M. L., Bich, G. A., Zapata, P. D., & Villalba, L. L. (2020). Trichoderma in Argentina: State of art. Ecologia Austral, 30(1), 113–124. https://doi.org/10.25260/EA.20.30.1.0.945 DOI: https://doi.org/10.25260/EA.20.30.1.0.945

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(1), Article 121. https://doi.org/10.1186/1471-2164-14-121 DOI: https://doi.org/10.1186/1471-2164-14-121

Barnett, H. L., & Hunter, B. B. (1998). Illustrated genera of imperfect fungi. The American Phytopathological Society. APS Press.

Barúa, J. E., de la Cruz, M., de Pedro, N., Cautain, B., Hermosa, R., Cardoza, R. E., Gutiérrez, S., Monte, E., Vicente, F., & Collado, I. G. (2019). Synthesis of trichodermin derivatives and their antimicrobial and cytotoxic activities. Molecules, 24(20), Article 3811. https://doi.org/10.3390/molecules24203811 DOI: https://doi.org/10.3390/molecules24203811

Bettiol, W., & Morandi, M. A. B. (2009). Trichoderma in Brazil: history, research, commercialization and perspectives. The Meeting of the Working Group on Biological Control of Fungal and Bacterial Plant Pathogens IOBC/wprs Bulletin, 43, 235–237. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/143491/1/2009AA-079.pdf

Błaszczyk, L., Strakowska, J., Chełkowski, J., Gąbka-Buszek, A., & Kaczmarek, J. (2016). Trichoderma species occurring on wood with decay symptoms in mountain forests in Central Europe: genetic and enzymatic characterization. Journal of Applied Genetics, 57(3), 397–407. https://doi.org/10.1007/s13353-015-0326-1 DOI: https://doi.org/10.1007/s13353-015-0326-1

Brito, J. P. C., Ramada, M. H. S., Magalhães, M. T. Q., Silva, L. P., & Ulhoa, C. J. (2014). Peptaibols from Trichoderma asperellum TR356 strain isolated from Brazilian soil. SpringerPlus, 3(1), Article 600. https://doi.org/10.1186/2193-1801-3-600 DOI: https://doi.org/10.1186/2193-1801-3-600

Britos, R., & Jongdae, P. (Eds.) (2016). Ka’a He’e. Stevia rebaudiana (Bertoni) Bertoni. La dulce planta de Paraguay para el mundo. Alternativa para la diversificación de la finca. IPTA – KOPIA. Caacupé, Paraguay. https://www.researchgate.net/publication/312899595_Ka’a_he’e_Stevia_rebaudiana_Bertoni_Bertoni_La_dulce_planta_de_Paraguay_para_el_mundo_alternativa_para_la_diversificacion_de_la_finca

Cai, F., & Druzhinina, I. S. (2021). In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma. Fungal Diversity, 107, 1–69. https://doi.org/10.1007/s13225-020-00464-4 DOI: https://doi.org/10.1007/s13225-020-00464-4

Chagas, L. F. B., Chagas Junior, A. F., Fidelis, R. R., Carvalho Filho, M. R., & Miller, L. O. (2017). Trichoderma asperellum efficiency in soybean yield components. Comunicata Scientiae, 8(1), 165–169. https://doi.org/10.14295/CS.v8i1.1754 DOI: https://doi.org/10.14295/cs.v8i1.1754

Chaverri, P., Branco-Rocha, F., Jaklitsch, W., Gazis, R., Degenkolb, T., & Samuels, G. J. (2015). Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia, 107(3), 558–590. https://doi.org/10.3852/14-147 DOI: https://doi.org/10.3852/14-147

Chaverri, P., & Samuels, G. (2003). Hypocrea/Trichoderma (Ascomycota, Hypocreales, Hypocreaceae): species with green ascospores. Studies in Mycology, 48, 1–116. https://www.researchgate.net/profile/Priscila-Chaverri/publication/259188197_HypocreaTrichoderma_Ascomycota_Hypocreales_Hypocreaceae_Species_with_green_ascospores/links/02e7e52a487bdbc37c000000/Hypocrea-Trichoderma-Ascomycota-Hypocreales-Hypocreaceae-Species-with-greenascospores.pdf

Consolo, V. F., Mónaco, C. I., Cordo, C. A., & Salerno, G. L. (2012). Characterization of novel Trichoderma spp. isolates as a search for effective biocontrollers of fungal diseases of economically important crops in Argentina. World Journal of Microbiology and Biotechnology, 28(4), 1389–1398. https://doi.org/10.1007/s11274-011-0938-5 DOI: https://doi.org/10.1007/s11274-011-0938-5

Contreras-Cornejo, H. A., Macías-Rodríguez, L., del-Val, E., & Larsen, J. (2016). Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiology Ecology, 92(4), Article fiw036. https://doi.org/10.1093/femsec/fiw036 DOI: https://doi.org/10.1093/femsec/fiw036

Cubilla-Ríos, A. A., Ruíz-Díaz-Mendoza, D. D., Romero-Rodríguez, M. C., Flores-Giubi, M. E., & Barúa Chamorro, J. E. (2019). Antibiosis de proteínas y metabolitos en especies de Trichoderma contra aislamientos paraguayos de Macrophomina phaseolina. Agronomía Mesoamericana, 30(1), 63–77. https://doi.org/10.15517/am.v30i1.34423 DOI: https://doi.org/10.15517/am.v30i1.34423

Daniel, J. F. S., & Rodrigues Filho, E. (2007). Peptaibols of Trichoderma. Natural Product Reports, 24(5), 1128–1141. https://doi.org/10.1039/b618086h DOI: https://doi.org/10.1039/b618086h

Degenkolb, T., Dieckmann, R., Nielsen, K. F., Gräfenhan, T., Theis, C., Zafari, D., Chaverri, P., Ismaiel, A., Brückner, H., Von Döhren, H., Thrane, U., Petrini, O., & Samuels, G. J. (2008). The Trichoderma brevicompactum clade: A separate lineage with new species, new peptaibiotics, and mycotoxins. Mycological Progress, 7(3), 177–219. https://doi.org/10.1007/s11557-008-0563-3 DOI: https://doi.org/10.1007/s11557-008-0563-3

Di Lelio, I., Coppola, M., Comite, E., Molisso, D., Lorito, M., Woo, S. L., Pennacchio, F., Rao, R., & Digilio, M. C. (2021). Temperature differentially influences the capacity of Trichoderma species to induce plant defense responses in tomato against insect pests. Frontiers in Plant Science, 12, Article 678830. https://doi.org/10.3389/fpls.2021.678830 DOI: https://doi.org/10.3389/fpls.2021.678830

Druzhinina, I. S., Kopchinskiy, A. G., Komoń, M., Bissett, J., Szakacs, G., & Kubicek, C. P. (2005). An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genetics and Biology, 42(10), 813–828. https://doi.org/10.1016/j.fgb.2005.06.007 DOI: https://doi.org/10.1016/j.fgb.2005.06.007

Druzhinina, I., & Kubicek, C. P. (2005). Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters? Journal of Zhejiang University-Science B, 6(2), 100–112. https://doi.org/10.1631/jzus.2005.B0100 DOI: https://doi.org/10.1631/jzus.2005.B0100

Feitosa Y. B., Cruz-Magalhães V., Argolo-Filho R. C., Souza J. T., & Loguercio, L. L. (2019). Characterization of genetic diversity on tropical Trichoderma germplasm by sequencing of rRNA internal transcribed spacers. BMC Research Notes, 12, Article 663. https://doi.org/10.1186/s13104-019-4694-1 DOI: https://doi.org/10.1186/s13104-019-4694-1

Fernández Gamarra, M. A., Maidana Ojeda, M., & Enciso Maldonado, G. A. (2017). Identificación molecular y tasa de crecimiento de cepas nativas de Trichoderma spp. aisladas de la Región Norte del Paraguay. Investigación Agraria, 19(2), 127–132. https://doi.org/10.18004/investig.agrar.2017.diciembre.127-132 DOI: https://doi.org/10.18004/investig.agrar.2017.diciembre.127-132

Ferreira, F. V., Herrmann-Andrade, A. M., Calabrese, C. D., Bello, F., Vázquez, D., & Musumeci, M. A. (2020). Effectiveness of Trichoderma strains isolated from the rhizosphere of citrus tree to control Alternaria alternata, Colletotrichum gloeosporioides and Penicillium digitatum A21 resistant to pyrimethanil in post-harvest oranges (Citrus sinensis L. (Osbeck)). Journal of Applied Microbiology, 129(3), 712–727. https://doi.org/10.1111/jam.14657 DOI: https://doi.org/10.1111/jam.14657

Fraceto, L. F., Maruyama, C. R., Guilger, M., Mishra, S., Keswani, C., Singh, H. B., & Lima, R. (2018). Trichoderma harzianumbased novel formulations: potential applications for management of Next-Gen agricultural challenges. Journal of Chemical Technology and Biotechnology, 93(8), 2056–2063. https://doi.org/10.1002/jctb.5613 DOI: https://doi.org/10.1002/jctb.5613

Galante, Y. M., De Conti, A., & Monteverdi, R. (1998). Application of Trichoderma enzymes in the food and feed industries. In G. E. Harman, & C. P. Kubicek (Eds.), Trichoderma and Gliocladium, Volume 2. Enzymes, biological control and commercial applications (pp. 341–356). Taylor & Francis Ltd. https://books.google.com.co/books?hl=en&lr=&id=20NZDwAAQBAJ&oi=fnd&pg=PA327&dq=+Application+of+Trichoderma+enzymes&ots=QYtPa5-D8b&sig=h5NYpOlEzR0APKh62ntzeSoY4WY&redir_esc=y#v=onepage&q=Application%20of%20Trichoderma%20enzymes&f=false DOI: https://doi.org/10.1201/9781482267945-23

Garcete Gómez, J. M., & Orrego Fuente, A. L. (2011). Efecto de aislados nativos de Trichoderma spp. en la incidencia de Macrophomina phaseolina (Tassi) Goid en sésamo (Sesamum indicum L.). Investigacion Agraria, 13(2), 87–93.https://www.agr.una.py/revista/index.php/ria/article/view/220

Haouhach, S., Karkachi, N., Oguiba, B., Sidaoui, A., Chamorro, I., Kihal, M., & Monte, E. (2020). Three new reports of Trichoderma in Algeria: T. atrobrunneum, (South) T. longibrachiatum (South), and T. afroharzianum (Northwest). Microorganisms, 8(10), Article 1455. https://doi.org/10.3390/microorganisms8101455 DOI: https://doi.org/10.3390/microorganisms8101455

Hermosa, M. R., Keck, E., Chamorro, I., Rubio, B., Sanz, L., Vizcaíno, J. A., Grondona, I., & Monte, E. (2004). Genetic diversity shown in Trichoderma biocontrol isolates. Mycological Research, 108(8), 897–906. https://doi.org/10.1017/S0953756204000358 DOI: https://doi.org/10.1017/S0953756204000358

Holmes, K. A., Shroers, H. -J., Thomas, S. E., Evans, H. C., & Samuels, G. J. (2004). Taxonomy and biocontrol potential of a new species of Trichoderma from the Amazon basin of South America. Mycological Progress, 3(3), 199–210. https://doi.org/10.1007/s11557-006-0090-z DOI: https://doi.org/10.1007/s11557-006-0090-z

Horta, M. A. C., Ferreira Filho, J. A., Murad, N. F., Santos, E. O., Santos, C. A., Mendes, J. S., Brandão, M. M., Azzoni, S. F., & Souza, A. P. (2018). Network of proteins, enzymes and genes linked to biomass degradation shared by Trichoderma species. Scientific Reports, 8(1), Article 1341. https://doi.org/10.1038/s41598-018-19671-w DOI: https://doi.org/10.1038/s41598-018-19671-w

Howell, C. R. (2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Disease, 87(1), 4–10. https://doi.org/10.1094/PDIS.2003.87.1.4 DOI: https://doi.org/10.1094/PDIS.2003.87.1.4

Inglis, P. W., Mello, S. C. M., Martins, I., Silva, J. B. T., Macêdo, K., Sifuentes, D. N., & Valadares-Inglis, M. C. (2020). Trichoderma from Brazilian garlic and onion crop soils and description of two new species: Trichoderma azevedoi and Trichoderma peberdyi. PLoS ONE, 15(3), Article e0228485. https://doi.org/10.1371/journal.pone.0228485 DOI: https://doi.org/10.1371/journal.pone.0228485

Jaklitsch, W. M. (2011). European species of Hypocrea part II: species with hyaline ascospores. Fungal Diversity, 48(1), 1–250. https://doi.org/10.1007/s13225-011-0088-y DOI: https://doi.org/10.1007/s13225-011-0088-y

Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166. https://doi.org/10.1093/bib/bbx108 DOI: https://doi.org/10.1093/bib/bbx108

Kubicek, C. P., Steindorff, A. S., Chenthamara, K., Manganiello, G., Henrissat, B., Zhang, J., Cai, F., Kopchinskiy, A. G., Kubicek, E. M., Kuo, A., Baroncelli, R., Sarrocco, S., Noronha, E. F., Vannacci, G., Shen, Q., Grigoriev, I. V., & Druzhinina, I. S. (2019). Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics, 20(1), Article 485. https://doi.org/10.1186/s12864-019-5680-7 DOI: https://doi.org/10.1186/s12864-019-5680-7

Kuhls, K., Lieckfeldt, E., Börner, T., & Guého, E. (1999). Molecular reidentification of human pathogenic Trichoderma isolates as Trichoderma longibrachiatum and Trichoderma citrinoviride. Medical Mycology, 37(1), 25–33. https://doi.org/10.1080/02681219980000041 DOI: https://doi.org/10.1080/02681219980000041

Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096 DOI: https://doi.org/10.1093/molbev/msy096

Li, M., Ma, G., Lian, H., Su, X. , Tian, Y., Huang, W., Mei, J., & Jiang, X. (2019). The effects of Trichoderma on preventing cucumber fusarium wilt and regulating cucumber physiology. Journal of Integrative Agriculture, 18(3), 607–617. https://doi.org/10.1016/S2095-3119(18)62057-X DOI: https://doi.org/10.1016/S2095-3119(18)62057-X

Lisboa, D. S., Santos, C., Barbosa, R. N., Magalhães, O., Paiva, L. M., Moreira, K. A., Lima, N., & Souza Motta, C. M. (2017). Requalification of a Brazilian Trichoderma collection and screening of its capability to decolourise real textile effluent. International Journal of Environmental Research and Public Health, 14(4), Article 373. https://doi.org/10.3390/ijerph14040373 DOI: https://doi.org/10.3390/ijerph14040373

Lombardi, N., Vitale, S., Turra, D., Reverberi, M., Fanelli, C., Vinale, F., Marra, R., Ruocco, M., Pascale, A., D’Errico, G., Woo, S. L., & Lorito, M. (2018). Root exudates of stressed plants stimulate and attract Trichoderma soil fungi. Molecular Plant- Microbe Interactions, 31(10), 982–994. https://doi.org/10.1094/MPMI-12-17-0310-R DOI: https://doi.org/10.1094/MPMI-12-17-0310-R

Lopes, F. A. C., Steindorff, A. S., Geraldine, A. M., Brandão, R. S., Monteiro, V. N., Lobo Júnior, M., Coelho, A. S. G., Ulhoa, C. J., & Silva, R. N. (2012). Biochemical and metabolic profiles of Trichoderma strains isolated from common bean crops in the Brazilian Cerrado, and potential antagonism against Sclerotinia sclerotiorum. Fungal Biology, 116(7), 815–824. https://doi.org/10.1016/j.funbio.2012.04.015 DOI: https://doi.org/10.1016/j.funbio.2012.04.015

López-Quintero, C. A., Atanasova, L., Franco-Molano, A. E., Gams, W., Komon-Zelazowska, M., Theelen, B., Müller, W. H., Boekhout, T., & Druzhinina, I. (2013). DNA barcoding survey of Trichoderma diversity in soil and litter of the Colombian lowland Amazonian rainforest reveals Trichoderma strigosellum sp. nov. and other species. Antonie van Leeuwenhoek, 104(5), 657–674. https://doi.org/10.1007/s10482-013-9975-4 DOI: https://doi.org/10.1007/s10482-013-9975-4

Macena, A. M. F., Kobori, N. N., Mascarin, G. M., Vida, J. B., & Hartman, G. L. (2020). Antagonism of Trichoderma-based biofungicides against Brazilian and North American isolates of Sclerotinia sclerotiorum and growth promotion of soybean. BioControl, 65(2), 235–246. https://doi.org/10.1007/s10526-019-09976-8 DOI: https://doi.org/10.1007/s10526-019-09976-8

Malmierca, M. G., Cardoza, R. E., Alexander, H. J., McCormick, S. P., Hermosa, R., Monte, E., & Gutiérrez, S. (2012). Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Applied and Environmental Microbiology, 78(14), 4856–4868. https://doi.org/10.1128/aem.00385-12 DOI: https://doi.org/10.1128/AEM.00385-12

Mayo-Prieto, S., Campelo, M. P., Lorenzana, A., Rodríguez-González, A., Reinoso, B., Gutiérrez, S., & Casquero, P. A. (2020). Antifungal activity and bean growth promotion of Trichoderma strains isolated from seed vs soil. European Journal of Plant Pathology, 158, 817–828. https://doi.org/10.1007/s10658-020-02069-8 DOI: https://doi.org/10.1007/s10658-020-02069-8

McSpadden Gardener, B. B., & Fravel, D. R. (2002). Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Progress, 3(1), 17. https://doi.org/10.1094/php-2002-0510-01-rv DOI: https://doi.org/10.1094/PHP-2002-0510-01-RV

Morán-Diez, M. E., Tranque, E., Bettiol, W., Monte, E., & Hermosa, R. (2020). Differential response of tomato plants to the application of three Trichoderma species when evaluating the control of Pseudomonas syringae populations. Plants, 9(5), Article 626. https://doi.org/10.3390/plants9050626 DOI: https://doi.org/10.3390/plants9050626

Moreno-Ruiz, D., Lichius, A., Turrà, D., Di Pietro, A., & Zeilinger, S. (2020). Chemotropism assays for plant symbiosis and mycoparasitism related compound screening in Trichoderma atroviride. Frontiers in microbiology, 11, Article 601251. https://doi.org/10.3389/fmicb.2020.601251 DOI: https://doi.org/10.3389/fmicb.2020.601251

Murray, M. G., & Thompson, W. F. (1980). Nucleic acids research rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8(19), 4321–4326. https://doi.org/10.1093/nar/8.19.4321 DOI: https://doi.org/10.1093/nar/8.19.4321

Naseby, D. C., Pascual, J. A., & Lynch, J. M. (2000). Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. Journal of Applied Microbiology, 88(1), 161–169. https://doi.org/10.1046/j.1365-2672.2000.00939.x DOI: https://doi.org/10.1046/j.1365-2672.2000.00939.x

Nieto-Jacobo, M. F., Steyaert, J. M., Salazar-Badillo, F. B., Vi Nguyen, D., Rostás, M., Braithwaite, M., 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, Article 102. https://doi.org/10.3389/fpls.2017.00102 DOI: https://doi.org/10.3389/fpls.2017.00102

Ortellado Franco, B. M., & Orrego Fuente, A. L. (2013). Compatibilidad in vitro de aislados nativos de Trichoderma spp. con fungicidas para el tratamiento de semillas. Investigacion Agraria, 15(1), 15–22. http://scielo.iics.una.py/scielo.php?script=sci_arttext&pid=S2305-06832013000100003&lng=en&nrm=iso

Pappu, L. (2018). Enhanced rhizosphere competence of Trichoderma viride grown in solid state fermentation on corn cob residue. Archives of Phytopathology and Plant Protection, 51(9–10), 505–529. https://doi.org/10.1080/03235408.2018.1490236 DOI: https://doi.org/10.1080/03235408.2018.1490236

Patel, J., Teli, B., Bajpai, R., Meher, J., Rashid, M., Mukherjee, A., & Yadav, S. K. (2019). Trichoderma mediated biocontrol and growth promotion in plants: an endophytic approach. In A. Kumar, A. Kishore Singh, & K. Kumar Choudary (Eds.), Role of plant growth promoting microorganisms in sustainable agriculture and nanotechnology (pp. 219–239). Woodhead Publishing. https://doi.org/10.1016/b978-0-12-817004-5.00013-0 DOI: https://doi.org/10.1016/B978-0-12-817004-5.00013-0

Raja, H. A., Miller, A. N., Pearce, C. J., & Oberlies, N. H. (2017). Fungal identification using molecular tools: a primer for the natural products research community. Journal of Natural Products, 80(3), 756–770. https://doi.org/10.1021/acs.jnatprod.6b01085 DOI: https://doi.org/10.1021/acs.jnatprod.6b01085

Richter, S., Cormican, M. G., Pfaller, M. A., Lee, C. K., Gingrich, R., Rinaldi, M. G., & Sutton, D. A. (1999). Fatal disseminated Trichoderma longibrachiatum infection in an adult bone marrow transplant patient: species identification and review of the literature. Journal of Clinical Microbiology, 37(4), 1154–1160. https://doi.org/10.1128/jcm.37.4.1154-1160.1999 DOI: https://doi.org/10.1128/JCM.37.4.1154-1160.1999

Rivera-Méndez, W., Obregón, M., Morán-Diez, M. E., Hermosa, R., & Monte, E. (2020). Trichoderma asperellum biocontrol activity and induction of systemic defenses against Sclerotium cepivorum in onion plants under tropical climate conditions. Biological Control, 141, Article 104145. https://doi.org/10.1016/j.biocontrol.2019.104145 DOI: https://doi.org/10.1016/j.biocontrol.2019.104145

Samuels, G. J. (2006). Trichoderma: Systematics, the sexual state, and ecology. Phytopathology, 96(2), 195–206. https://doi.org/10.1094/PHYTO-96-0195 DOI: https://doi.org/10.1094/PHYTO-96-0195

Samuels, G. J., Dodd, S., Lu, B. S., Petrini, O., Schroers, H. J., & Druzhinina, I. S. (2006). The Trichoderma koningii aggregate species. Studies in Mycology, 56(1), 67–133. https://doi.org/10.3114/sim.2006.56.03 DOI: https://doi.org/10.3114/sim.2006.56.03

Samuels, G. J., & Hebbar, P. K. (2015). Trichoderma: identification and agricultural applications. APS Press. https://my.apsnet.org/ItemDetail?iProductCode=44846

Sanabria Velázquez, A. D. (2020). Evaluación de aislados de Trichoderma spp. nativos del Paraguay para el control de Colletotrichum spp. causante de la antracnosis en frutilla. Investigacion Agraria, 22(1), 53–62. https://doi.org/10.18004/investig.agrar.2020.junio.53-62 DOI: https://doi.org/10.18004/investig.agrar.2020.junio.53-62

Sanabria Velazquez, A. D., & Grabowski Ocampos, C. J. (2016). Control biológico de Rosellinia sp. causante de la muerte súbita en macadamia (Macadamia integrifolia) con aislados de Trichoderma spp. Investigacion Agraria, 18(2), 77–86. https://www.agr.una.py/revista/index.php/ria/article/view/306 DOI: https://doi.org/10.18004/investig.agrar.2016.diciembre.77-86

Sarsaiya, S., Jain, A., Fan, X., Jia, Q., Xu, Q., Shu, F., Zhou, Q., Shi, J., & Chen, J. (2020). New insights into detection of a dendrobine compound from a novel endophytic Trichoderma longibrachiatum strain and its toxicity against phytopathogenic bacteria. Frontiers in Microbiology, 11, Article 337. https://doi.org/10.3389/fmicb.2020.00337 DOI: https://doi.org/10.3389/fmicb.2020.00337

Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A., Chen, W., Bolchacova, E., Voigt, K., Crous, P. W., Miller, A. N., Wingfield, M. J., Aime, M. C., An, K. D., Bai, F. Y., Barreto, R. W., Begerow, D., Bergeron, M. J., Blackwell, M., …, & Schindel, D. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America, 109(16), 6241–6246. https://doi.org/10.1073/pnas.1117018109 DOI: https://doi.org/10.1073/pnas.1207508109

Sempere Ferre, F., & Santamarina, M. P. (2010). Efficacy of Trichoderma harzianum in suppression of Fusarium culmorum. Annals of Microbiology, 60(2), 335–340. https://doi.org/10.1007/s13213-010-0047-y DOI: https://doi.org/10.1007/s13213-010-0047-y

Shi, W. L., Chen, X. L., Wang, L. X., Gong, Z. T., Li, S., Li, C. L., Xie, B. B., Zhang, W., Shi, M., Li, C., Zhang, Y. Z., & Song, X. Y. (2016). Cellular and molecular insight into the inhibition of primary root growth of Arabidopsis induced by peptaibols, a class of linear peptide antibiotics mainly produced by Trichoderma spp. Journal of Experimental Botany, 67(8), 2191–2205. https://doi.org/10.1093/jxb/erw023 DOI: https://doi.org/10.1093/jxb/erw023

Silva, R. N., Steindorff, A. S., & Monteiro, V. N. (2014). Metabolic diversity of Trichoderma. In V. K. Gupta, M. Schmoll, A. Herrera-Estrella, R. S. Upadhyay, I. Druzhinina, & M. G. Tuohy (Eds.), Biotechnology and Biology of Trichoderma (pp. 363–376). Elsevier. https://doi.org/10.1016/B978-0-444-59576-8.00027-8 DOI: https://doi.org/10.1016/B978-0-444-59576-8.00027-8

Stauffer Bonzon, A. (1999). Obtención de aislados de Trichoderma sp. a nivel local y su efecto en el control de hongos fitopatogénicos. Informe de Investigación. Dirección General de Investigaciones Cientificas y Tecnológicas, Universidad Nacional de Asunción. https://www.cnc.una.py/opac/cliente.cgi?codbiblio=DGICT&orderby=&mode=full&last_mode=brief&last_limit=15&last_next_rec=1&last_cclquery=au%3D%28Stauffer+or+Bonzon%29&last_codbiblio=TODAS&last_cant_total_reg=29&cclquery=ln%3D205664914&sintaxis=XML

Stielow, J. B., Lévesque, C. A., Seifert, K. A., Meyer, W., Irinyi, L., Smits, D., Renfurm, R., Verkley, G. J. M., Groenewald, M., Chaduli, D., Lomascolo, A., Welti, S., Lesage-Meessen, L., Favel, A., Al-Hatmi, A. M. S., Damm, U., Yilmaz, N., Houbraken, J., Lombard, L., …, & Robert, V. (2015). One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes. Persoonia - Molecular Phylogeny and Evolution of Fungi, 35(1), 242–263. https://doi.org/10.3767/003158515X689135 DOI: https://doi.org/10.3767/003158515X689135

Tijerino, A., Hermosa, R., Cardoza, R. E., Moraga, J., Malmierca, M. G., Aleu, J., Collado, I. G., Monte, E., & Gutierrez, S. (2011). Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins, 3(9), 1220–1232. https://doi.org/10.3390/toxins3091220 DOI: https://doi.org/10.3390/toxins3091220

Woo, S. L., Ruocco, M., Vinale, F., Nigro, M., Marra, R., Lombardi, N., Pascale, A., Lanzuise, S., Manganiello, G., & Lorito, M. (2014). Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal, 8(Supp1), 71–126. https://doi.org/10.2174/1874437001408010071 DOI: https://doi.org/10.2174/1874437001408010071

Wu, Q., Sun, R., Ni, M., Yu, J., Li, Y., Yu, C., Dou, K., Ren, J., & Chen, J. (2017). Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLoS ONE, 12(6), Article e0179957. https://doi.org/10.1371/journal.pone.0179957 DOI: https://doi.org/10.1371/journal.pone.0179957

Yendyo, S., Ramesh, G. C., & Pandey, B. R. (2017). Evaluation of Trichoderma spp., Pseudomonas fluorescence and Bacillus subtilis for biological control of Ralstonia wilt of tomato. F1000Research, 6, Article 2028. https://doi.org/10.12688%2Ff1000research.12448.3 DOI: https://doi.org/10.12688/f1000research.12448.1

Zhang, S., Xu, B., Zhang, J., & Gan, Y. (2018). Identification of the antifungal activity of Trichoderma longibrachiatum T6 and assessment of bioactive substances in controlling phytopathgens. Pesticide Biochemistry and Physiology, 147, 59–66. https://doi.org/10.1016/j.pestbp.2018.02.006 DOI: https://doi.org/10.1016/j.pestbp.2018.02.006

How to Cite

APA

Sanabria-Velázquez, A. D., Florentín Pavía, M. M., Insaurralde Ayala, L., Flores-Giubi, M. E., Romero-Rodríguez, M. C., Sotelo, P. H. and Barúa, J. E. (2023). Characterization of Trichoderma species from agricultural soils of Paraguay. Agronomía Colombiana, 41(3), e111299. https://doi.org/10.15446/agron.colomb.v41n3.111299

ACM

[1]
Sanabria-Velázquez, A.D., Florentín Pavía, M.M., Insaurralde Ayala, L., Flores-Giubi, M.E., Romero-Rodríguez, M.C., Sotelo, P.H. and Barúa, J.E. 2023. Characterization of Trichoderma species from agricultural soils of Paraguay. Agronomía Colombiana. 41, 3 (Sep. 2023), e111299. DOI:https://doi.org/10.15446/agron.colomb.v41n3.111299.

ACS

(1)
Sanabria-Velázquez, A. D.; Florentín Pavía, M. M.; Insaurralde Ayala, L.; Flores-Giubi, M. E.; Romero-Rodríguez, M. C.; Sotelo, P. H.; Barúa, J. E. Characterization of Trichoderma species from agricultural soils of Paraguay. Agron. Colomb. 2023, 41, e111299.

ABNT

SANABRIA-VELÁZQUEZ, A. D.; FLORENTÍN PAVÍA, M. M.; INSAURRALDE AYALA, L.; FLORES-GIUBI, M. E.; ROMERO-RODRÍGUEZ, M. C.; SOTELO, P. H.; BARÚA, J. E. Characterization of Trichoderma species from agricultural soils of Paraguay. Agronomía Colombiana, [S. l.], v. 41, n. 3, p. e111299, 2023. DOI: 10.15446/agron.colomb.v41n3.111299. Disponível em: https://revistas.unal.edu.co/index.php/agrocol/article/view/111299. Acesso em: 19 jul. 2024.

Chicago

Sanabria-Velázquez, Andrés Dejesús, Marcos Marcelo Florentín Pavía, Lorena Insaurralde Ayala, María Eugenia Flores-Giubi, María Cristina Romero-Rodríguez, Pablo Hernán Sotelo, and Javier E. Barúa. 2023. “Characterization of Trichoderma species from agricultural soils of Paraguay”. Agronomía Colombiana 41 (3):e111299. https://doi.org/10.15446/agron.colomb.v41n3.111299.

Harvard

Sanabria-Velázquez, A. D., Florentín Pavía, M. M., Insaurralde Ayala, L., Flores-Giubi, M. E., Romero-Rodríguez, M. C., Sotelo, P. H. and Barúa, J. E. (2023) “Characterization of Trichoderma species from agricultural soils of Paraguay”, Agronomía Colombiana, 41(3), p. e111299. doi: 10.15446/agron.colomb.v41n3.111299.

IEEE

[1]
A. D. Sanabria-Velázquez, “Characterization of Trichoderma species from agricultural soils of Paraguay”, Agron. Colomb., vol. 41, no. 3, p. e111299, Sep. 2023.

MLA

Sanabria-Velázquez, A. D., M. M. Florentín Pavía, L. Insaurralde Ayala, M. E. Flores-Giubi, M. C. Romero-Rodríguez, P. H. Sotelo, and J. E. Barúa. “Characterization of Trichoderma species from agricultural soils of Paraguay”. Agronomía Colombiana, vol. 41, no. 3, Sept. 2023, p. e111299, doi:10.15446/agron.colomb.v41n3.111299.

Turabian

Sanabria-Velázquez, Andrés Dejesús, Marcos Marcelo Florentín Pavía, Lorena Insaurralde Ayala, María Eugenia Flores-Giubi, María Cristina Romero-Rodríguez, Pablo Hernán Sotelo, and Javier E. Barúa. “Characterization of Trichoderma species from agricultural soils of Paraguay”. Agronomía Colombiana 41, no. 3 (September 1, 2023): e111299. Accessed July 19, 2024. https://revistas.unal.edu.co/index.php/agrocol/article/view/111299.

Vancouver

1.
Sanabria-Velázquez AD, Florentín Pavía MM, Insaurralde Ayala L, Flores-Giubi ME, Romero-Rodríguez MC, Sotelo PH, Barúa JE. Characterization of Trichoderma species from agricultural soils of Paraguay. Agron. Colomb. [Internet]. 2023 Sep. 1 [cited 2024 Jul. 19];41(3):e111299. Available from: https://revistas.unal.edu.co/index.php/agrocol/article/view/111299

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