Histochemical changes induced by Trichoderma spp. and potassium phosphite in common bean (Phaseolus vulgaris) in response to the attack by Colletotrichum lindemuthianum
DOI:
https://doi.org/10.5433/1679-0359.2020v41n3p811Keywords:
Anthracnose, Hypersensitivity response. Induction of resistance, Oxygen-reactive species.Abstract
Induction of resistance in common bean (Phaseolus vulgaris) has been considered a promising alternative to control anthracnose. Among the changes generated in the induction of resistance, structural changes have been reported by several authors as an efficient form of resistance to the stress plants undergo. Histochemical analysis techniques have been used to investigate tissue changes triggered by induction of resistance. Thus, this study aims to investigate certain histochemical changes suffered by common bean plants induced with potassium phosphite and Trichoderma spp. in response to the attack by Colletotrichum lindemuthianum, aiming to determine the host response pattern in terms of structural changes, associating it to possible disease control. Treatments consisted of isolates T. harzianum (isolate TOD1) and T. virens (isolate TM4), leaf fertilizer potassium phosphite Fertilis®, and distilled water (control). Inducers were applied to common bean alone or associated, consisting of five treatments plus the control treatment. The six treatments were evaluated for the absence and presence of C. lindemuthianum in a factorial scheme (6×2). Treatments allowed evaluating the severity of anthracnose in common bean, location of H2O2, lignin deposition, and hypersensitivity response in common bean hypocotyl by histochemical staining. Potassium phosphite and combinations of T. virens and T. harzianum with potassium phosphite efficiently reduced disease severity under greenhouse conditions, reaching 68, 84, and 71%, respectively. Studies with hypocotyl showed that T. harzianum + potassium phosphite and T. virens + potassium phosphite accelerated the H2O2 accumulation process and lignin deposition at the pathogen penetration site, in addition to the hypersensitivity reaction through the resistance-inducing activity, contributing to the protection of common bean against anthracnose caused by C. lindemuthianum.Downloads
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References
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Baxter, H. L., & Stewart, C. N. (2013). Effects of altered lignin biosynthesis on phenylpropanoid metabolism and plant stress. Biofuels, 4(6), 635-650. doi: 10.4155/bfs.13.56
Borges, A. A., & Sandalio, L. S. (2015). Induced resistance for plant defense. Frontiers in Plant Science, 6(109), 109-124. doi: 10.3389/fpls.2015.00109
Costa, B. H. G., Resende, M. L. V., Monteiro, A. C. A., Ribeiro, P. M. Jr., Botelho, D. M. S., & Silva, B. M. (2017). Potassium phosphites in the protection of common bean plants against anthracnose and biochemical defence responses. Journal of Phytopathology, 166(2), 1-8. doi: 10.1111/jph.12665
Cruz, M. F. A., Araujo, L., Polanco, L. R. & Rodrigues, F. A. (2014). Aspectos microscópicos da interação feijoeiro Colletotrichum lindemuthianum mediados pelo silício. Bragantia, 73(3), 284-291. doi: 10.1590/1678-4499.0139
Dalla Pria, M., Amorim, L., & Bergamin, A., Filho. (2003). Quantificação de componentes monocíclicos da antracnose do feijoeiro. Fitopatologia Brasileira, 28(4), 401-407, 2003. doi: 10.1590/S0100-41582003000400009
Dalla Pria, M., Amorin, L., & Canteri, M. G. (1999). Métodos de avaliação das doenças. In: Canteri, M. G., Dalla Pria, M., & Silva, O. C. Principais doenças fúngicas do feijoeiro (pp. 53-64). Ponta Grossa: UEPG.
Dildey, O. D. F. (2014). Interação Trichoderma-feijoeiro e seus efeitos na fisiologia e indução de resistência contra antracnose (Colletotrichum lindemuthianum). Dissertação de mestrado, Universidade Estadual do Oeste do Paraná, Marechal Candido Rondon, PR, Brasil. Recuperado de http://tede.unioeste.br/
Dordas, C. (2008). Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agronomy for Sustainable Development, 28(1), 33-46. doi: 10.1051/agro:2007051
Eshraghi, L., Anderson, J., Aryamanesh, N., Shearer, B., Mccomb, J., G. E., Hardya, S. J., & O’briena, P. A. (2011). Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathology, 60, 1086-1095. doi: 10.1111/j.1365-3059.2011.02471.x
Fontenelle, A. D. B., Guzzo, S. D., Lucon, C. M. M., & Harakava, R. (2011). Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp. Crop Protection, 30(11), 1492-1500. doi: 10.1016/j.cropro.2011.07.019
Freitas, M. B., & Stadnik, M. J. (2012). Race-specific and ulvan-induced defense responses in bean (Phaseolus vulgaris) against Colletotrichum lindemuthianum. Physiological and Molecular Plant Pathology, 78, 8-13. doi: 10.1016/j.pmpp.2011.12.004
Gadaga, S. J. C., Abreu, M. S., Resende, M. L. V., & Ribeiro, P. M., Jr. (2017). Phosphites for the control of anthracnose in common bean. Pesquisa Agropecuária Brasileira, 52(1), 36-44. doi: 10.1590/S0100-204X2017000100005
Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930. doi: 10.1016/j.plaphy.2010.08.016
Gómez-Merino, F. G., & Trejo-Téllez, L. I. (2015). Biostimulant activity of phosphite in horticulture. Scientia Horticulturae, 196(30), 82-90. doi: 10.1016/j.scienta.2015.09.035
Jwa, N. S., & Hwang, B. K. (2017). Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Frontiers in Plant Science, 8(1687), 1-12. doi: 10.3389/fpls.2017.01687
Kumudini, B. S., Vasanthi, N. S., & Shetty, H. S. (2001). Hypersensitive response, cell death and histochemical localization of hydrogen peroxide in host and non-host seedlings infected with the downy mildew pathogen Sclerospora graminicola. Annals of Applied Biology, 139(2), 217-225. doi: 10.111/j.1744-7348.2001.tb00398.x
Melo, T. A., Araújo, M. U. P., Serra, I. M. R. S., & Pascholati, S. F. (2017). Produtos naturais disponíveis comercialmente induzem o acúmulo de fitoalexinas em cotilédones de soja e mesocótilos de sorgo. Summa Phytopathologica, 43(3), 205-211. doi: 10.1590/0100-5405/167358
Niranjan Raj, A. S., Lavanya, A. S. N., Amruthesh, A. K. N., Niranjana, A. S. R., & Reddy, B. H. S. (2012). Histo-chemical changes induced by PGPR during induction of resistance in pearl millet against downy mildew disease. Biological Control, 60(2), 90-102. doi: 10.1016/j.biocontrol.2011.10.011
Nojosa, G. B. R. A., Resende, M. L. V., Barguil, B. M., Moraes, S. R. G., & Vilas Boas, C. H. (2009). Efeito de indutores de resistência em cafeeiro contra a mancha de Phoma. Summa Phytopathologica, 35(1), 60-62. doi: 10.159/S0100-54052009000100011
Nozaki, M. H., & Kliemann, O. A. (2016). Avaliação do uso de fosfito no controle da antracnose em feijoeiro comum. Revista Agrarian, 9(31), 19-25. Recuperado de http://ojs.ufgd.edu.br/index.php/agrarian/article/view/3076/3633
O’Connell, K. J., Bailey, J. A., & Richmond, D. V. (1985). Cytology and physiology of infection of Phaseolus vulgaris by Colletotrichum lindemuthianum. Physiological Plant Pathology, 27(1), 75-98. doi: 10.1016/0048-4059(85)90058-X
Pedro, A. S., Harakava, R., Lucon, C. M. M., & Guzzo, S. D. (2012). Promoção do crescimento do feijoeiro e controle da antracnose por Trichoderma spp. Pesquisa Agropecuária Brasileira, 47(11), 1589-1595. doi: 10.1590/S0100-204X2012001100005
Saba, H., Vibhash, D., Manisha, M., Prashant, K. S., Farhan, H., & Tauseef A. (2012). Trichoderma- a promising plant growth stimulator and biocontrol agent. Mycosphere, 3(4), 524-531. doi: 10.5943/mycosphere/3/4/14
Statistical Analysis System Institute (2014). SAS University edition. Users Guide. Cary: SAS Institute INC.
Sewelam, N., Kazan, K., & Schenk, P. M. (2016). Global plant stress signaling: reactive oxygen species at the cross-road. Frontiers in Plant Science, 7(187), 1-21. doi: 10.3389/fpls.2016.00187
Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilization on the expression of slow-mildewing resistence in knox wheat. Phytopathology, 67(8), 1051-1056. doi: 10.1094/Phyto-67-1051
Silva, H. F., Pinto, K. M. S., Nascimento, L. C., Silva, E. C., & Souza, W. C. O. (2019). Avaliação do uso de elicitores de resistência bióticos e abióticos contra a antracnose na videira (Vitis labrusca L.). Summa Phytopathologica, 45(1), 70-75. doi: 10.1590/0100-5405/180414
Silva, J. L., Souza, P. E., Alves, E., Pinto, J. E. B. P., Bertolucci, S. K. V., Freitas, M. L. O., & Resende, M. L. V. (2015). Essential oil of Cymbopogon flexuosus, Vernonia polyanthes and potassium phosphite in control of bean anthracnose. Journal of Medicinal Plants Research, 9(8), 243-253. doi: 10.5897/JMPR2014.5718
Silva, L. M., Alquini, Y., & Cavallet, V. J. (2005). Inter-relações entre a anatomia vegetal e a produção vegetal. Acta Botanica Brasílica, 19(1), 183-194. doi: 10.1590/S0102-33062005000100018
Singh, A., Shukla, N., Kabadwal, B. C., Tewari, A. K., & Kumar, J. (2018). Review on plant-Trichoderma-pathogen interaction. International Journal of Current Microbiology and Applied Sciences, 7(2), 2382-2397. doi: 10.20546/ijcmas.2018.702.291
Soares, A. M. S., & Machado, O. L. T. (2007). Defesa de plantas: sinalização química e espécies reativas de oxigênio. Revista Trópica: Ciências Agrárias e Biológicas, 1(1), 9-19. Recuperado de https://www.academia.edu/6571798/Defesa_De_Plantas_Sinalizacao_Quimica_EEspecies_Reativas_De_Oxigenio_bio_Ar
Southerton, S. G., & Deverall, B. J. (1990). Histochemical and chemical evidence for lignin accumulation during the expression of resistance to leaf rust fungi in wheat. Physiological and Molecular Plant Pathology, 36(6), 483-494. doi: 10.1016/0885-5765(90)90021-O
Stangarlin, J. R., Kuhn, O. J., Toledo, M. V., Portz, R. L., Schwan-Estrada, K. R. F., & Pascholati, S. F. (2011). A defesa vegetal contra fitopatógenos. Scientia Agraria Paranaensis, 10(1), 18-46. doi: 10.1818/sap.v10i1.5268
Stangarlin, J. R., Schulz, D. G., Franzener, G., Assi, L., Schwan-Estrada, K. R. F., & Kuhn, O. J. (2010). Indução de fitoalexinas em soja e sorgo por preparações de Saccharomyces boulardii. Arquivos do Instituto Biológico, 77(1), 91-98. Recuperado de https://www.researchgate.net/publication/324574822
Tavares, G. M., Laranjeira, D., Luz, E. D. M. N., Silva, T. R., Pirovani, C. P., Resende, M. L. V., & Ribeiro, P. M., Jr. (2009). Indução de resistência do mamoeiro à podridão radicular por indutores bióticos e abióticos. Pesquisa Agropecuária Brasileira, 44(11), 1416-1423. doi: 10.1590/S0100-204X2009001100007
Thordal-Christensen, H., Zhang, Z., Wei, Y., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. The Plant Journal, 11(6), 1187-1194. doi: 10.1046/j.1365-313X.1997.11061187.x
Walters, D. R., Ratsep, J., & Havis, N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. Journal of Experimental Botany, 64(5), 1263-1280. doi: 10.1093/jxb/ert026
Zurbriggen, M. D., Carrillo, N., & Hajirezaei, M. (2010). ROS signaling in the hypersensitive response. Plant Signaling and Behavior, 5(4), 393-396. doi: 10.4161/psb.5.4.10793
Baldo, M., Stangarlin, J. R., Franzener, G., Assi, L., Kuhn, O. J., & Schwan-Estrada, K. R. F. (2011). Detecção in situ de espécies reativas de oxigênio em feijoeiro tratado com extratos de Pycnoporus sanguineus e inoculado com Colletotrichum lindemuthianum. Summa Phytopathologica, 37(4), 174-179. doi: 10.1590/S0100-54052011000400002
Bashir, Z., Ahmad, A., Shafique, S., Anjum, T., Shafique, S., & Akram, W. (2013). Hypersensitive response - A biophysical phenomenon of producers. European Journal of Microbiology and Immunology, 3(2), 105-110. doi: 10.1556/EuJMI.3.2013.2.3
Baxter, H. L., & Stewart, C. N. (2013). Effects of altered lignin biosynthesis on phenylpropanoid metabolism and plant stress. Biofuels, 4(6), 635-650. doi: 10.4155/bfs.13.56
Borges, A. A., & Sandalio, L. S. (2015). Induced resistance for plant defense. Frontiers in Plant Science, 6(109), 109-124. doi: 10.3389/fpls.2015.00109
Costa, B. H. G., Resende, M. L. V., Monteiro, A. C. A., Ribeiro, P. M. Jr., Botelho, D. M. S., & Silva, B. M. (2017). Potassium phosphites in the protection of common bean plants against anthracnose and biochemical defence responses. Journal of Phytopathology, 166(2), 1-8. doi: 10.1111/jph.12665
Cruz, M. F. A., Araujo, L., Polanco, L. R. & Rodrigues, F. A. (2014). Aspectos microscópicos da interação feijoeiro Colletotrichum lindemuthianum mediados pelo silício. Bragantia, 73(3), 284-291. doi: 10.1590/1678-4499.0139
Dalla Pria, M., Amorim, L., & Bergamin, A., Filho. (2003). Quantificação de componentes monocíclicos da antracnose do feijoeiro. Fitopatologia Brasileira, 28(4), 401-407, 2003. doi: 10.1590/S0100-41582003000400009
Dalla Pria, M., Amorin, L., & Canteri, M. G. (1999). Métodos de avaliação das doenças. In: Canteri, M. G., Dalla Pria, M., & Silva, O. C. Principais doenças fúngicas do feijoeiro (pp. 53-64). Ponta Grossa: UEPG.
Dildey, O. D. F. (2014). Interação Trichoderma-feijoeiro e seus efeitos na fisiologia e indução de resistência contra antracnose (Colletotrichum lindemuthianum). Dissertação de mestrado, Universidade Estadual do Oeste do Paraná, Marechal Candido Rondon, PR, Brasil. Recuperado de http://tede.unioeste.br/
Dordas, C. (2008). Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agronomy for Sustainable Development, 28(1), 33-46. doi: 10.1051/agro:2007051
Eshraghi, L., Anderson, J., Aryamanesh, N., Shearer, B., Mccomb, J., G. E., Hardya, S. J., & O’briena, P. A. (2011). Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathology, 60, 1086-1095. doi: 10.1111/j.1365-3059.2011.02471.x
Fontenelle, A. D. B., Guzzo, S. D., Lucon, C. M. M., & Harakava, R. (2011). Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp. Crop Protection, 30(11), 1492-1500. doi: 10.1016/j.cropro.2011.07.019
Freitas, M. B., & Stadnik, M. J. (2012). Race-specific and ulvan-induced defense responses in bean (Phaseolus vulgaris) against Colletotrichum lindemuthianum. Physiological and Molecular Plant Pathology, 78, 8-13. doi: 10.1016/j.pmpp.2011.12.004
Gadaga, S. J. C., Abreu, M. S., Resende, M. L. V., & Ribeiro, P. M., Jr. (2017). Phosphites for the control of anthracnose in common bean. Pesquisa Agropecuária Brasileira, 52(1), 36-44. doi: 10.1590/S0100-204X2017000100005
Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930. doi: 10.1016/j.plaphy.2010.08.016
Gómez-Merino, F. G., & Trejo-Téllez, L. I. (2015). Biostimulant activity of phosphite in horticulture. Scientia Horticulturae, 196(30), 82-90. doi: 10.1016/j.scienta.2015.09.035
Jwa, N. S., & Hwang, B. K. (2017). Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Frontiers in Plant Science, 8(1687), 1-12. doi: 10.3389/fpls.2017.01687
Kumudini, B. S., Vasanthi, N. S., & Shetty, H. S. (2001). Hypersensitive response, cell death and histochemical localization of hydrogen peroxide in host and non-host seedlings infected with the downy mildew pathogen Sclerospora graminicola. Annals of Applied Biology, 139(2), 217-225. doi: 10.111/j.1744-7348.2001.tb00398.x
Melo, T. A., Araújo, M. U. P., Serra, I. M. R. S., & Pascholati, S. F. (2017). Produtos naturais disponíveis comercialmente induzem o acúmulo de fitoalexinas em cotilédones de soja e mesocótilos de sorgo. Summa Phytopathologica, 43(3), 205-211. doi: 10.1590/0100-5405/167358
Niranjan Raj, A. S., Lavanya, A. S. N., Amruthesh, A. K. N., Niranjana, A. S. R., & Reddy, B. H. S. (2012). Histo-chemical changes induced by PGPR during induction of resistance in pearl millet against downy mildew disease. Biological Control, 60(2), 90-102. doi: 10.1016/j.biocontrol.2011.10.011
Nojosa, G. B. R. A., Resende, M. L. V., Barguil, B. M., Moraes, S. R. G., & Vilas Boas, C. H. (2009). Efeito de indutores de resistência em cafeeiro contra a mancha de Phoma. Summa Phytopathologica, 35(1), 60-62. doi: 10.159/S0100-54052009000100011
Nozaki, M. H., & Kliemann, O. A. (2016). Avaliação do uso de fosfito no controle da antracnose em feijoeiro comum. Revista Agrarian, 9(31), 19-25. Recuperado de http://ojs.ufgd.edu.br/index.php/agrarian/article/view/3076/3633
O’Connell, K. J., Bailey, J. A., & Richmond, D. V. (1985). Cytology and physiology of infection of Phaseolus vulgaris by Colletotrichum lindemuthianum. Physiological Plant Pathology, 27(1), 75-98. doi: 10.1016/0048-4059(85)90058-X
Pedro, A. S., Harakava, R., Lucon, C. M. M., & Guzzo, S. D. (2012). Promoção do crescimento do feijoeiro e controle da antracnose por Trichoderma spp. Pesquisa Agropecuária Brasileira, 47(11), 1589-1595. doi: 10.1590/S0100-204X2012001100005
Saba, H., Vibhash, D., Manisha, M., Prashant, K. S., Farhan, H., & Tauseef A. (2012). Trichoderma- a promising plant growth stimulator and biocontrol agent. Mycosphere, 3(4), 524-531. doi: 10.5943/mycosphere/3/4/14
Statistical Analysis System Institute (2014). SAS University edition. Users Guide. Cary: SAS Institute INC.
Sewelam, N., Kazan, K., & Schenk, P. M. (2016). Global plant stress signaling: reactive oxygen species at the cross-road. Frontiers in Plant Science, 7(187), 1-21. doi: 10.3389/fpls.2016.00187
Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilization on the expression of slow-mildewing resistence in knox wheat. Phytopathology, 67(8), 1051-1056. doi: 10.1094/Phyto-67-1051
Silva, H. F., Pinto, K. M. S., Nascimento, L. C., Silva, E. C., & Souza, W. C. O. (2019). Avaliação do uso de elicitores de resistência bióticos e abióticos contra a antracnose na videira (Vitis labrusca L.). Summa Phytopathologica, 45(1), 70-75. doi: 10.1590/0100-5405/180414
Silva, J. L., Souza, P. E., Alves, E., Pinto, J. E. B. P., Bertolucci, S. K. V., Freitas, M. L. O., & Resende, M. L. V. (2015). Essential oil of Cymbopogon flexuosus, Vernonia polyanthes and potassium phosphite in control of bean anthracnose. Journal of Medicinal Plants Research, 9(8), 243-253. doi: 10.5897/JMPR2014.5718
Silva, L. M., Alquini, Y., & Cavallet, V. J. (2005). Inter-relações entre a anatomia vegetal e a produção vegetal. Acta Botanica Brasílica, 19(1), 183-194. doi: 10.1590/S0102-33062005000100018
Singh, A., Shukla, N., Kabadwal, B. C., Tewari, A. K., & Kumar, J. (2018). Review on plant-Trichoderma-pathogen interaction. International Journal of Current Microbiology and Applied Sciences, 7(2), 2382-2397. doi: 10.20546/ijcmas.2018.702.291
Soares, A. M. S., & Machado, O. L. T. (2007). Defesa de plantas: sinalização química e espécies reativas de oxigênio. Revista Trópica: Ciências Agrárias e Biológicas, 1(1), 9-19. Recuperado de https://www.academia.edu/6571798/Defesa_De_Plantas_Sinalizacao_Quimica_EEspecies_Reativas_De_Oxigenio_bio_Ar
Southerton, S. G., & Deverall, B. J. (1990). Histochemical and chemical evidence for lignin accumulation during the expression of resistance to leaf rust fungi in wheat. Physiological and Molecular Plant Pathology, 36(6), 483-494. doi: 10.1016/0885-5765(90)90021-O
Stangarlin, J. R., Kuhn, O. J., Toledo, M. V., Portz, R. L., Schwan-Estrada, K. R. F., & Pascholati, S. F. (2011). A defesa vegetal contra fitopatógenos. Scientia Agraria Paranaensis, 10(1), 18-46. doi: 10.1818/sap.v10i1.5268
Stangarlin, J. R., Schulz, D. G., Franzener, G., Assi, L., Schwan-Estrada, K. R. F., & Kuhn, O. J. (2010). Indução de fitoalexinas em soja e sorgo por preparações de Saccharomyces boulardii. Arquivos do Instituto Biológico, 77(1), 91-98. Recuperado de https://www.researchgate.net/publication/324574822
Tavares, G. M., Laranjeira, D., Luz, E. D. M. N., Silva, T. R., Pirovani, C. P., Resende, M. L. V., & Ribeiro, P. M., Jr. (2009). Indução de resistência do mamoeiro à podridão radicular por indutores bióticos e abióticos. Pesquisa Agropecuária Brasileira, 44(11), 1416-1423. doi: 10.1590/S0100-204X2009001100007
Thordal-Christensen, H., Zhang, Z., Wei, Y., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. The Plant Journal, 11(6), 1187-1194. doi: 10.1046/j.1365-313X.1997.11061187.x
Walters, D. R., Ratsep, J., & Havis, N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. Journal of Experimental Botany, 64(5), 1263-1280. doi: 10.1093/jxb/ert026
Zurbriggen, M. D., Carrillo, N., & Hajirezaei, M. (2010). ROS signaling in the hypersensitive response. Plant Signaling and Behavior, 5(4), 393-396. doi: 10.4161/psb.5.4.10793
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2020-04-07
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Figueira, E. P. P., Kuhn, O. J., Martinazzo-Portz, T., Stangarlin, J. R., Pereira, M. D. P., & Lampugnani, C. (2020). Histochemical changes induced by Trichoderma spp. and potassium phosphite in common bean (Phaseolus vulgaris) in response to the attack by Colletotrichum lindemuthianum. Semina: Ciências Agrárias, 41(3), 811–828. https://doi.org/10.5433/1679-0359.2020v41n3p811
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