Biosolubilização de fosfatos por cepas de Trichoderma in vitro e em invernada sobre três variedades de Coffea arabica
Palavras-chave:
fungos solubilizadores de fosfato (PSF), plantas do café, biofertilização
Resumo
Os solos cafeeiros apresentam baixa disponibilidade de fósforo, o uso de cepas de Trichoderma solubilizadoras de fosfato é uma estratégia sustentável promissora para o manejo das deficiências de fósforo. Neste estudo no México, avaliamos cepas 10 Trichoderma do solos andossolos de plantações de café no México e sua capacidade de solubilização de fosfato in vitro, e seu impacto no crescimento de mudas de café de três variedades (Anacafé, Costa Rica e Marsellesa). Os microrganismos testados apresentaram solubilização de fósforo variou entre 2,41 e 7,40 mg.mL-1. A máxima atividade solubilizadora de fosfato foi observada utilizando duas cepas de Trichoderma harzianum 75,73 (Th53) e 74,62 mg.mL-1 (Th48) para fosfato de cálcio (Ca2PO4) e três cepas de T. asperellum 22,99 (Th57), 22,90 (Th49) e 21,55 mg.mL-1(Th40) para fosfato de alumínio (AlPO4). Tanto no fosfato de cálcio (Ca2PO4) quanto no fosfato de alumínio (AlPO4) foi detectada diminuição do pH do meio, de 4,81 para 3,73 e de 3,38 para 2,75, respectivamente. Na variedade Anacafé, a aplicação de duas cepas de T. harzianum (Th48 e Th53) favoreceu maior disponibilidade de fósforo no substrato, enquanto nas variedades Costa Rica e Marseillaise o fósforo disponível do substrato foi maior com T. harzianum (Th48 ). A inoculação com estas cepas de Trichoderma é potencialmente importante para a solubilização do fósforo insolúvel e o desenvolvimento dos cafeeiros.
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Referências
Arias, R. M., & Heredia, G. (2014). Fungal diversity in coffee plantation systems and in a tropical montane cloud forest in Veracruz, Mexico. Agroforestry systems, 88, 921-933. https://doi.org/10.1007/s10457-014-9736-z
Arias, R. M., Heredia, G., Perea-Rojas, Y. del C., de la Cruz, E.Y., & García G. K. Y. (2023). Selection and characterization of phosphate-solubilizing fungi and their effects on coffee plantations. Plants, 12(19), 3395. https://doi.org/10.3390/plants12193395
Arias, R. M., Juárez, G.A., Heredia, G., & de la Cruz, E. Y. (2022). Capacidad fosfato solubilizadora de hongos rizosféricos provenientes de cafetales de Jilotepec, Veracruz. Alianzas y Tendencias BUAP, 7(27), 6986. http://doi.org/10.5281/zenodo.7094878
Bader, A. N., Salerno, G. L., Covacevich, F., & Consolo, V. F. (2020). Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). Journal of King Saud University Science, 32(1), 867–873. https://doi.org/10.1016/j.jksus.2019.04.002
Bononi, L., Chiaramonte, J. B., Pansa, C. C., Moitinho, M. A., & Melo, I. S. (2020). Phosphorus-solubilizing Trichoderma spp. from Amazon soils improve soybean plant growth. Scientific Reports, 10(1), 2858. https://doi.org/10.1038/s41598-020-59793-8
Bray, R. H., & Kurtz. L. T. (1945). Determination of total, organic and available forms of phosphorus in soil. Soil Science, 59, 39-45. DOI:10.1097/00010694-194501000-00006
Cano, M. 2015. Interacción de microorganismos benéficos en plantas: Micorrizas, Trichoderma spp. y Pseudomonas spp. una revisión. Revista U.D.C.A Actualidad & Divulgación Científica, 14(2), 15-31.
Chagas, L. F. B., De Castro, H. G., Colonia, B. S. O., De Carvalho Filho, M. R., Miller, L. D. O., & Chagas, A. F. J. (2016). Efficiency of Trichoderma spp. as a growth promoter of cowpea (Vigna unguiculata) and analysis of phosphate solubilization and indole acetic acid synthesis. Brazilian Journal of Botany, 39(2), 437-445. https://doi.org/10.1007/s40415-015-0247-6
Clesceri, S., Greenberg, A., & Trusell, R. (1992). Métodos normalizados para el análisis de aguas potables y residuales. 17th ed. Madrid: Ediciones Díaz de Santos.
Galeano, R. M. S., Ribeiro, J. V. S., Silva, S. M., de Oliveira-Simas, A. L., de Alencar-Guimarães, N. C., Masui, D. C., Corrêa, B. O., Giannesi, G. C., Ferreira de Lima, S., da Silva-Brasil, M., & Zanoelo, F. F. (2024). New strains of Trichoderma with potential for biocontrol and plant growth promotion improve early soybean growth and development. Journal Plant Growth Regulation, 43, 4099–4119. https://doi.org/10.1007/s00344-024-11374-z
Gams, W., & Bissett, J. (2002). Morphology and identification of Trichoderma Vol 1. Basic biology, taxonomy and genetics. In P. C. Kubicek & G. E. Harman (Eds.), Trichoderma and Gliocladium (pp. 3-31). Taylor and Francis.
Geissert, D., & Ibañez, A. (2008). Calidad y ambiente físico-químico de los suelos. In R. Manson, V. Hernández-Ortiz, S. Gallina & K. Mehltreter (Eds.), Agrosistemas cafetaleros de Veracruz: Biodiversidad, Manejo y Conservación (pp. 213-221). Instituto de Ecología, A.C. (INECOL) e Instituto Nacional de Ecología (INE-SEMARNAT).
Hernández-Leal, T. I., Carrión, G., & Heredia, G. (2011). In vitro phosphate solubilization by a strain of Paecilomyces lilacinus (Thom) Samson. Agrociencia, 45(8), 881-892. https://www.scielo.org.mx/scielo.php?pid=S1405-31952011000800003&script=sci_abstract&tlng=en
Huerta, P. G., & Holguín, M. (2019). La microbiota del cafetal, modulador del daño producido por insectos y enfermedades. In B. E. Bello, L. Soto Pinto, P. G. Huerta, R. J. Gómez (Eds.), Caminar el cafetal: perspectivas socioambientales del café y su gente (pp. 49-64). El Colegio de la Frontera Sur. https://biblioteca.ecosur.mx/cgi-bin/koha/opac-retrieve-file.pl?id=29766d1b642f4ea743b565b20e921ff6
Kaissoumi, H. E. L., Berbera, F., Mouden, N., OuazzaniChandi, A., Ouazzani, T. A., Selmaoui, K., Benkirane, R., & Douira, A. (2024). Tomato growth promotion by Trichoderma asperellum laboratory-made bioproduct. In M. Azrour, J. Mabrouki & A. Guezzaz. (Eds.), Sustainable and Green Technologies for Water and Environmental Management (pp. 161-171). World Sustainability Series. Springer, Cham. https://doi.org/10.1007/978-3-031-52419-6_13
Kribel, S., Qostal, S., Ouazzani-Touhami, A., Selmaoui, K., Chliyeh, M., Benkirane, R., Achbani, E. H., & Douira, A. (2019). Qualitative and quantitative estimation of the ability of Trichoderma spp. Moroccan isolates to solubilize tricalcium phosphate. Plant Cell Biotechnology and Molecular Biology, 20 (7-8), 275-284. DOI: 10.1556/038.54.2019.016
Li, R. X., Cai, F., Pang, G., Shen, Q. S., Li, R., & Chen, W. (2015). Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One, 10(6), e0130081. https://doi.org/10.1371/journal.pone.0130081
Liebersbach, H., Steingrobe, B., & Claassen, N. (2004). Roots regulate ion transport in the rhizosphere to counteract reduced mobility in dry soil. Plant and Soil, 260, 79-88. https://doi.org/10.1023/B:PLSO.0000030191.92338.6a
Menezes-Blackburn, D., Paredes, C., Zhang, H., Giles, C. D., Darch, T., Stutter, M., George, T. S., Shand, C., Lumsdon, D., Cooper, P., Wendler, R., Brown, L., Blackwell, M., Wearing, C., & Haygarth, P. M. (2016). Organic acids regulation of chemical–microbial phosphorus transformations in soils. Environmental Science & Technology Journal, 50(21), 11521–11531. 10.1021/acs.est.6b03017 https://pubs.acs.org/doi/10.1021/acs.est.6b03017
Mulatu, A., Megersa, N., Abena, T., Kanagarajan, S., Liu, Q., Tenkegna, T. A., & Vetukuri, R. R. (2022). Biodiversity of the genus Trichoderma in the rhizosphere of coffee (Coffea arabica) plants in Ethiopia and their potential use in biocontrol of coffee wilt disease. Crops, 2(2), 120-141. https://doi.org/10.3390/crops2020010
National Center for Biotechnology Information (NCBI). (2024). Trichoderma Internal Transcribed Spacer RNA (ITS), Fungal Internal Transcribed Spacer RNA (ITS) RefSeq Targeted Loci Project. Available online: https://www.ncbi.nlm.nih.gov/nuccore/?term=Trichoderma+its+type (Consulted january 2024).
Oliveros-Bastidas, A. D. J., Macías, F. A., Fernández, C. C., Marín, D., & Molinillo, J. M. (2009). Exudados de la raíz y su relevancia actual en las interacciones alelopáticas. Química Nova, 32, 198-213. https://doi.org/10.1590/S0100-40422009000100035
Osorno, L., & Osorio, N. (2014). Effect of carbon and nitrogen source and concentration on rock phosphate dissolution induced by fungi. Journal of Applied Biotechnology, 2(2), 32-42. 10.5296/jab.v2i2.5475 https://www.macrothink.org/journal/index.php/jab/article/view/5475
Perea-Rojas, Y. C., Arias, R. M., Medel, Ortiz, R., Trejo, A. D., Heredia, G., & Rodríguez, Y. Y. (2019). Effects of native arbuscular mycorrhizal and phosphate-solubilizing fungi on coffee plants. Agroforestry Systems, 93, 961–972. https://doi.org/10.1007/s10457-018-0190-1
Pikovskaya, R. I. (1948). Mobilization of phosphorus in soil in con-nection with vital activity of some microbial species. Mikrobiologiya, 17, 362-70.
Prasad, A., Dixit, M., Meena, S. K., & Kumar, A. (2023). Qualitative and quantitative estimation for phosphate solubilizing ability of Trichoderma isolates: A natural soil health enhancer. Materials Today: Proceedings, 81, 360-366. https://doi.org/10.1016/j.matpr.2021.03.305
Sadeghian, S., Alarcon, V. F., Díaz-Poveda, V., Lince-Salazar, L. A., & Rey-Sandoval, J. C. (2019). Fertilidad del suelo y manejo de la nutrición. En Centro Nacional de Investigaciones de Café (Ed.), Aplicación de ciencia tecnología e innovación en el cultivo del café ajustado a las condiciones particulares del Huila (pp. 80–105). Cenicafé. https://doi.org/10.38141/10791/0005_4
Souchie, E., Azcón, R., Barea, J., Silva, E., Saggin-Júnior, O. (2010). Enhancement of clover growth by inoculation of P-solubilizing fungi and arbuscular mycorrhizal fungi. Anais da Academia Brasileira de Ciências, 82(3), 771-777. https://www.scielo.br/j/aabc/a/88xv7fcjktmPnkshbm6xGJF/?lang=en
Tandon, A., Fatima, T., Shukla, D., Tripathi, P., Srivastava, S., & Singh, P. C. (2020). Phosphate solubilization by Trichoderma koningiopsis (NBRI-PR5) under abiotic stress conditions. Journal of King Saud University, 32(1), 791-798. https://doi.org/10.1016/j.jksus.2019.02.001
White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D.H. Gelfand, J. J. Sninsky & T. J. White (Eds), PCR protocols: a guide to methods and applications (pp. 315-322). Academic Press.
Yang, T., Li, L., Wang, B., Tian, J., Shi, F., Zhang, S., & Wu, Z. (2022). Isolation, mutagenesis, and organic acid secretion of a highly efficient phosphate-solubilizing fungus. Frontiers in Microbiology, 13, 793122. https://doi.org/10.3389/fmicb.2022.793122
Zhang, Y., Chen, F.S., Wu, X.Q., Luan, F.G., Zhang, L.P., Fang, X.M., Wan, S.Z., Hu, X.F., & Ye, J.R. (2018). Isolation and characterization of two phosphate-solubilizing fungi from rhizosphere soil of moso bamboo and their functional capacities when exposed to different phosphorus sources and pH environments. PLoS One, 13(7), e0199625. https://doi.org/10.1371/journal.pone.0199625
Zin, N. A., & Badaluddin, N. A. (2020). Biological functions of Trichoderma spp. for agriculture applications. Annals of Agricultural Sciences, 65(2), 168-178. https://doi.org/10.1016/j.aoas.2020.09.003
Arias, R. M., Heredia, G., Perea-Rojas, Y. del C., de la Cruz, E.Y., & García G. K. Y. (2023). Selection and characterization of phosphate-solubilizing fungi and their effects on coffee plantations. Plants, 12(19), 3395. https://doi.org/10.3390/plants12193395
Arias, R. M., Juárez, G.A., Heredia, G., & de la Cruz, E. Y. (2022). Capacidad fosfato solubilizadora de hongos rizosféricos provenientes de cafetales de Jilotepec, Veracruz. Alianzas y Tendencias BUAP, 7(27), 6986. http://doi.org/10.5281/zenodo.7094878
Bader, A. N., Salerno, G. L., Covacevich, F., & Consolo, V. F. (2020). Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). Journal of King Saud University Science, 32(1), 867–873. https://doi.org/10.1016/j.jksus.2019.04.002
Bononi, L., Chiaramonte, J. B., Pansa, C. C., Moitinho, M. A., & Melo, I. S. (2020). Phosphorus-solubilizing Trichoderma spp. from Amazon soils improve soybean plant growth. Scientific Reports, 10(1), 2858. https://doi.org/10.1038/s41598-020-59793-8
Bray, R. H., & Kurtz. L. T. (1945). Determination of total, organic and available forms of phosphorus in soil. Soil Science, 59, 39-45. DOI:10.1097/00010694-194501000-00006
Cano, M. 2015. Interacción de microorganismos benéficos en plantas: Micorrizas, Trichoderma spp. y Pseudomonas spp. una revisión. Revista U.D.C.A Actualidad & Divulgación Científica, 14(2), 15-31.
Chagas, L. F. B., De Castro, H. G., Colonia, B. S. O., De Carvalho Filho, M. R., Miller, L. D. O., & Chagas, A. F. J. (2016). Efficiency of Trichoderma spp. as a growth promoter of cowpea (Vigna unguiculata) and analysis of phosphate solubilization and indole acetic acid synthesis. Brazilian Journal of Botany, 39(2), 437-445. https://doi.org/10.1007/s40415-015-0247-6
Clesceri, S., Greenberg, A., & Trusell, R. (1992). Métodos normalizados para el análisis de aguas potables y residuales. 17th ed. Madrid: Ediciones Díaz de Santos.
Galeano, R. M. S., Ribeiro, J. V. S., Silva, S. M., de Oliveira-Simas, A. L., de Alencar-Guimarães, N. C., Masui, D. C., Corrêa, B. O., Giannesi, G. C., Ferreira de Lima, S., da Silva-Brasil, M., & Zanoelo, F. F. (2024). New strains of Trichoderma with potential for biocontrol and plant growth promotion improve early soybean growth and development. Journal Plant Growth Regulation, 43, 4099–4119. https://doi.org/10.1007/s00344-024-11374-z
Gams, W., & Bissett, J. (2002). Morphology and identification of Trichoderma Vol 1. Basic biology, taxonomy and genetics. In P. C. Kubicek & G. E. Harman (Eds.), Trichoderma and Gliocladium (pp. 3-31). Taylor and Francis.
Geissert, D., & Ibañez, A. (2008). Calidad y ambiente físico-químico de los suelos. In R. Manson, V. Hernández-Ortiz, S. Gallina & K. Mehltreter (Eds.), Agrosistemas cafetaleros de Veracruz: Biodiversidad, Manejo y Conservación (pp. 213-221). Instituto de Ecología, A.C. (INECOL) e Instituto Nacional de Ecología (INE-SEMARNAT).
Hernández-Leal, T. I., Carrión, G., & Heredia, G. (2011). In vitro phosphate solubilization by a strain of Paecilomyces lilacinus (Thom) Samson. Agrociencia, 45(8), 881-892. https://www.scielo.org.mx/scielo.php?pid=S1405-31952011000800003&script=sci_abstract&tlng=en
Huerta, P. G., & Holguín, M. (2019). La microbiota del cafetal, modulador del daño producido por insectos y enfermedades. In B. E. Bello, L. Soto Pinto, P. G. Huerta, R. J. Gómez (Eds.), Caminar el cafetal: perspectivas socioambientales del café y su gente (pp. 49-64). El Colegio de la Frontera Sur. https://biblioteca.ecosur.mx/cgi-bin/koha/opac-retrieve-file.pl?id=29766d1b642f4ea743b565b20e921ff6
Kaissoumi, H. E. L., Berbera, F., Mouden, N., OuazzaniChandi, A., Ouazzani, T. A., Selmaoui, K., Benkirane, R., & Douira, A. (2024). Tomato growth promotion by Trichoderma asperellum laboratory-made bioproduct. In M. Azrour, J. Mabrouki & A. Guezzaz. (Eds.), Sustainable and Green Technologies for Water and Environmental Management (pp. 161-171). World Sustainability Series. Springer, Cham. https://doi.org/10.1007/978-3-031-52419-6_13
Kribel, S., Qostal, S., Ouazzani-Touhami, A., Selmaoui, K., Chliyeh, M., Benkirane, R., Achbani, E. H., & Douira, A. (2019). Qualitative and quantitative estimation of the ability of Trichoderma spp. Moroccan isolates to solubilize tricalcium phosphate. Plant Cell Biotechnology and Molecular Biology, 20 (7-8), 275-284. DOI: 10.1556/038.54.2019.016
Li, R. X., Cai, F., Pang, G., Shen, Q. S., Li, R., & Chen, W. (2015). Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One, 10(6), e0130081. https://doi.org/10.1371/journal.pone.0130081
Liebersbach, H., Steingrobe, B., & Claassen, N. (2004). Roots regulate ion transport in the rhizosphere to counteract reduced mobility in dry soil. Plant and Soil, 260, 79-88. https://doi.org/10.1023/B:PLSO.0000030191.92338.6a
Menezes-Blackburn, D., Paredes, C., Zhang, H., Giles, C. D., Darch, T., Stutter, M., George, T. S., Shand, C., Lumsdon, D., Cooper, P., Wendler, R., Brown, L., Blackwell, M., Wearing, C., & Haygarth, P. M. (2016). Organic acids regulation of chemical–microbial phosphorus transformations in soils. Environmental Science & Technology Journal, 50(21), 11521–11531. 10.1021/acs.est.6b03017 https://pubs.acs.org/doi/10.1021/acs.est.6b03017
Mulatu, A., Megersa, N., Abena, T., Kanagarajan, S., Liu, Q., Tenkegna, T. A., & Vetukuri, R. R. (2022). Biodiversity of the genus Trichoderma in the rhizosphere of coffee (Coffea arabica) plants in Ethiopia and their potential use in biocontrol of coffee wilt disease. Crops, 2(2), 120-141. https://doi.org/10.3390/crops2020010
National Center for Biotechnology Information (NCBI). (2024). Trichoderma Internal Transcribed Spacer RNA (ITS), Fungal Internal Transcribed Spacer RNA (ITS) RefSeq Targeted Loci Project. Available online: https://www.ncbi.nlm.nih.gov/nuccore/?term=Trichoderma+its+type (Consulted january 2024).
Oliveros-Bastidas, A. D. J., Macías, F. A., Fernández, C. C., Marín, D., & Molinillo, J. M. (2009). Exudados de la raíz y su relevancia actual en las interacciones alelopáticas. Química Nova, 32, 198-213. https://doi.org/10.1590/S0100-40422009000100035
Osorno, L., & Osorio, N. (2014). Effect of carbon and nitrogen source and concentration on rock phosphate dissolution induced by fungi. Journal of Applied Biotechnology, 2(2), 32-42. 10.5296/jab.v2i2.5475 https://www.macrothink.org/journal/index.php/jab/article/view/5475
Perea-Rojas, Y. C., Arias, R. M., Medel, Ortiz, R., Trejo, A. D., Heredia, G., & Rodríguez, Y. Y. (2019). Effects of native arbuscular mycorrhizal and phosphate-solubilizing fungi on coffee plants. Agroforestry Systems, 93, 961–972. https://doi.org/10.1007/s10457-018-0190-1
Pikovskaya, R. I. (1948). Mobilization of phosphorus in soil in con-nection with vital activity of some microbial species. Mikrobiologiya, 17, 362-70.
Prasad, A., Dixit, M., Meena, S. K., & Kumar, A. (2023). Qualitative and quantitative estimation for phosphate solubilizing ability of Trichoderma isolates: A natural soil health enhancer. Materials Today: Proceedings, 81, 360-366. https://doi.org/10.1016/j.matpr.2021.03.305
Sadeghian, S., Alarcon, V. F., Díaz-Poveda, V., Lince-Salazar, L. A., & Rey-Sandoval, J. C. (2019). Fertilidad del suelo y manejo de la nutrición. En Centro Nacional de Investigaciones de Café (Ed.), Aplicación de ciencia tecnología e innovación en el cultivo del café ajustado a las condiciones particulares del Huila (pp. 80–105). Cenicafé. https://doi.org/10.38141/10791/0005_4
Souchie, E., Azcón, R., Barea, J., Silva, E., Saggin-Júnior, O. (2010). Enhancement of clover growth by inoculation of P-solubilizing fungi and arbuscular mycorrhizal fungi. Anais da Academia Brasileira de Ciências, 82(3), 771-777. https://www.scielo.br/j/aabc/a/88xv7fcjktmPnkshbm6xGJF/?lang=en
Tandon, A., Fatima, T., Shukla, D., Tripathi, P., Srivastava, S., & Singh, P. C. (2020). Phosphate solubilization by Trichoderma koningiopsis (NBRI-PR5) under abiotic stress conditions. Journal of King Saud University, 32(1), 791-798. https://doi.org/10.1016/j.jksus.2019.02.001
White, T. J., Bruns, T., Lee, S., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D.H. Gelfand, J. J. Sninsky & T. J. White (Eds), PCR protocols: a guide to methods and applications (pp. 315-322). Academic Press.
Yang, T., Li, L., Wang, B., Tian, J., Shi, F., Zhang, S., & Wu, Z. (2022). Isolation, mutagenesis, and organic acid secretion of a highly efficient phosphate-solubilizing fungus. Frontiers in Microbiology, 13, 793122. https://doi.org/10.3389/fmicb.2022.793122
Zhang, Y., Chen, F.S., Wu, X.Q., Luan, F.G., Zhang, L.P., Fang, X.M., Wan, S.Z., Hu, X.F., & Ye, J.R. (2018). Isolation and characterization of two phosphate-solubilizing fungi from rhizosphere soil of moso bamboo and their functional capacities when exposed to different phosphorus sources and pH environments. PLoS One, 13(7), e0199625. https://doi.org/10.1371/journal.pone.0199625
Zin, N. A., & Badaluddin, N. A. (2020). Biological functions of Trichoderma spp. for agriculture applications. Annals of Agricultural Sciences, 65(2), 168-178. https://doi.org/10.1016/j.aoas.2020.09.003
Publicado
2024-11-18
Como Citar
Arias, R., Torres, A., Perea, Y., & Cruz, Y. (2024). Biosolubilização de fosfatos por cepas de Trichoderma in vitro e em invernada sobre três variedades de Coffea arabica. Revista Da Faculdade De Agronomia Da Universidade De Zulia, 41(4), e244241. Obtido de https://mail.produccioncientificaluz.org/index.php/agronomia/article/view/42932
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Produção Vegetal
Direitos de Autor (c) 2024 Rosa María Arias Mota, Alberto Donaldo Torres Salas, Yamel del Carmen Perea Rojas, Yadeneyro de la Cruz Elizondo
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