Published

2024-08-31

Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation

Hallazgos preliminares sobre el biocontrol del marchitamiento y cancro bacteriano del tomate (Clavibacter michiganensis subsp. michiganensis) utilizando Trichoderma harzianum luego de una biofumigaciòn

DOI:

https://doi.org/10.15446/agron.colomb.v42n2.114659

Keywords:

biological control, phytopathogenic bacteria, tomato yield, microbial antagonists (en)
control biológico, bacteria fitopatógena, rendimiento de tomate, antagonistas microbianos (es)

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Authors

  • Marina Stocco Universidad Nacional de la Plata - Facultad de Ciencias Agrarias y Forestales - Centro de Investigaciones de Fitopatología - La Plata, Argentina https://orcid.org/0009-0004-6764-8976
  • Jorgelina Rolleri Universidad Nacional de la Plata - Facultad de Ciencias Agrarias y Forestales - Centro de Investigaciones de Fitopatología - La Plata, Argentina / Ministerio de Desarrollo Agrario de la Provincia de Buenos Aires - Buenos Aires, Argentina https://orcid.org/0009-0007-6755-4015
  • Paulina Moya Universidad Nacional de Tierra del Fuego - Instituto de Ciencias Polares, Ambiente y Recursos Naturales - Tierra del Fuego, Argentina https://orcid.org/0009-0002-7306-6951
  • Julieta Peñalba Universidad Nacional de la Plata - Facultad de Ciencias Agrarias y Forestales - Centro de Investigaciones de Fitopatología - La Plata, Argentina https://orcid.org/0009-0009-6679-9242
  • Cecilia Mónaco Universidad Nacional de la Plata - Facultad de Ciencias Agrarias y Forestales - Centro de Investigaciones de Fitopatología - La Plata, Argentina https://orcid.org/0000-0003-3190-9260

One of the most aggressive bacterial diseases in tomato crops is bacterial wilt and canker caused by Clavibacter michiganensis subsp. michiganensis (Cmm). Chemical control is questioned due to its negative effects on health and the environment. Within integrated disease management, one alternative is biocontrol with Trichoderma species. Another technique is biofumigation, which releases volatile compounds into the soil that inhibit soil-borne fungi and stimulate plant health. The aim of this study was to evaluate the potential of biofumigation and the use of Trichoderma harzianum for the control of bacterial wilt and tomato canker caused by Cmm in vitro and their effect on yields in a commercial tomato crop. The inhibition of phytopathogenic bacteria of the in vitro test and the number and weight of fruits per plant in a greenhouse were evaluated. The treatments were: tomato plants inoculated with Cmm with or without two strains of T. harzianum, alone and in combination with biofumigation. The in vitro test results showed, with both strains, no significant differences between the treatments, although the growth of Cmm was lower in the combination biofumigation and T. harzianum. One of the strains of T. harzianum (Th118) performed better than the other for yield (weight and number of fruits). However, the results do not show a synergistic effect between T. harzianum and biofumigation in the observed yield values.

Una de las enfermedades bacterianas más agresivas en el cultivo de tomate es el marchitamiento y cancro bacteriano ocasionado por Clavibacter michiganensis subsp. michiganensis (Cmm). Su control químico es cuestionado por sus efectos negativos en la salud y el ambiente. Dentro de un manejo integrado de enfermedades una alternativa es el biocontrol con especies de Trichoderma. Otra técnica es la biofumigación que libera al suelo compuestos volátiles que inhiben fitopatógenos y favorecen la sanidad de las plantas. El objetivo del estudio fue evaluar el potencial de la biofumigación y el uso de Trichoderma harzianum para el control de la marchitez bacteriana y cancro del tomate causado por Cmm in vitro y observar el efecto sobre los rendimientos en un cultivo comercial. Se evaluó el número y peso de frutos por planta, donde los tratamientos fueron: plantas de tomates inoculadas con Cmm en presencia o ausencia de dos cepas de T. harzianum solas y en combinación con biofumigación. Los resultados de los ensayos in vitro mostraron que a pesar de que no hubo diferencias significativas entre los tratamientos, el crecimiento de Cmm fue menor en la combinación biofumigación y T. harzianum. Una de las cepas de T. harzianum, (Th118), tuvo mejor comportamiento que la otra, teniendo en cuenta el efecto sobre el rendimiento (peso y número de frutos). Por otro lado, los resultados no muestran un efecto sinérgico entre T. harzianum y la biofumigación en los valores de rendimiento observados.

References

Abo-Elyousr, K. A. M., Khalil Bagy, H. M. N., Hashem, M., Alamri, S. A. M., & Mostafa, Y. S. (2019). Biological control of the tomato wilt caused by Clavibacter michiganensis subsp. michiganensis using formulated plant growth-promoting bacteria. Egyptian Journal of Biological Pest Control, 29, Article 54. https://doi.org/10.1186/s41938-019-0152-6

Amerio, N. S., Castrillo, M. L., Bich, G. A., Zapata, P. D., & Villalba, L. M. (2020). Trichoderma en la Argentina: estado del arte. Ecología Austral, 30(1), 113–124. https://doi.org/10.25260/EA.20.30.1.0.945

Bakker, M. G., Glover, J. D., Mai, J. G., & Kinkel, L. L. (2010). Plant community effects on the diversity and pathogen suppressive activity of soil streptomycetes. Applied Soil Ecology, 46(1), 35–42. https://doi.org/10.1016/j.apsoil.2010.06.003

Berlanas, C., Andrés-Sodupe, M., López-Manzanares, B., Maldonado-González, M. M., & Gramaje, D. (2018). Effect of white mustard cover crop residue, soil chemical fumigation and Trichoderma spp. root treatment on black-foot disease control in grapevine. Pest Management Science, 74(12), 2864–2873. https://doi.org/10.1002/ps.5078

Bonanomi, G., Antignani, V., Capodilupo, M., & Scala, F. (2010). Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biology and Biochemistry, 42(2), 136–144. https://doi.org/10.1016/j.soilbio.2009.10.012

Brown, P. D., & Morra, M. J. (1997). Control of soil-borne plant pests using glucosinolate-containing plants. Advances in Agronomy, 61, 167–231. https://doi.org/10.1016/S0065-2113(08)60664-1

Chalupowicz, L., Barash, I., Reuven, M., Dror, O., Sharabani, G., Gartemann, K. H., Eichenlaub, R., Sessa, G., & Manulis-Sasson, S. (2016). Differential contribution of Clavibacter michiganensis ssp. michiganensis virulence factors to systemic and local infection in tomato. Molecular Plant Pathology, 18(3), 336–346. https://doi.org/10.1111/mpp.12400

Cordo, C. A., Mónaco, C. I., Segarra, C. I., Simon, M. R., Mansilla, A. Y., Perelló, A. E., Kripelz, N. I., Bayo, D., & Conde, R. D. (2007). Trichoderma spp. as elicitors in the defense responses of wheat plants against Septoria tritici. Biocontrol Science and Technology, 17(7), 687–698. https://doi.org/10.1080/09583150701527094

Dal Bello, G., Rollán, M. C., Lampugnani, G., Abramoff, C., Ronco, L., Larrán, S., Stocco, M., & Mónaco, C. (2011). Biological control of leaf grey mould of greenhouse tomatoes caused by Botrytis cinerea. International Journal of Pest Management, 57(2), 177–182. https://doi.org/10.1080/09670874.2011.561887

Daugovish, O., Thill, D. C., & Shafii, T. (2009). Modeling competition between wild oat (Avena fatua L.) and yellow mustard or canola. Weed Science, 51(1), 102–109. https://doi.org/10.1614/0043-1745(2003)051[0102:MCBWOA]2.0.CO;2

Davis, M. J., Gillaspie Jr., A. G., Vidaver, A. K., & Harris, R. (1984). Clavibacter: A new genus containing some phytopathogenic coryneform bacteria, including Clavibacter xyli subsp. xyli sp. nov., subsp. nov. and Cavibacter xyli subsp. cynodonis subsp. nov., pathogens that cause ratoon stunting disease of sugarcane and bermudagrass stunting disease. International Journal of Systematic Bacteriology, 34, 107–117. https://doi.org/10.1099/00207713-34-2-107

Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2020). InfoStat versión 2020. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

Dugassa, A., Alemu, T., & Woldehawariat, Y. (2021) In vitro compatibility assay of indigenous Trichoderma and Pseudomonas species and their antagonistic activities against black root rot disease (Fusarium solani) of faba bean (Vicia faba L.). BMC Microbiology, 21, Article 115. https://doi.org/10.1186/s12866-021-02181-7

EPPO-European and Mediterranean Plant Protection Organization. (2013). EPPO standards - Diagnostics - PM 7/42 (3) Clavibacter michiganensis subsp. michiganensis. EPPO Bulletin, 46(2), 202–225. https://www.eppo.int/RESOURCES/eppo_standards/pm7_diagnostics DOI: https://doi.org/10.1111/epp.12302

Galletti, S., Sala, E., Leoni, O., Burzi, P. L., & Cerato, C. (2008). Trichoderma spp. tolerance to Brassica carinata seed meal for a combined use in biofumigation. Biological Control, 45(3), 319–327. https://doi.org/10.1016/j.biocontrol.2008.01.014

Guzmán-Guzmán, P., Ajay Kumar, A., Santos-Villalobos, S., Parra-Cota, F. I., Orozco-Mosqueda, M. C., Fadiji, A. E., Hyder, S., Babalola O. O., & Santoyo, G. (2023). Trichoderma species: Our best fungal allies in the biocontrol of plant diseases – A review. Plants, 12(3), Article 432. https://doi.org/10.3390/plants12030432

Hanschen, F. S., & Winkelmann, T. (2020). Biofumigation for fighting replant disease – A review. Agronomy, 10(3), Article 425. https://doi.org/10.3390/agronomy10030425

Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species — Opportunistic, avirulent plant symbionts. Nature Reviews Microbiology, 2, 43–56. https://doi.org/10.1038/nrmicro797

Kawaguchi, A., Tanina, K., & Inoue, K. (2010). Molecular typing and spread of 625 Clavibacter michiganensis subsp. michiganensis in greenhouses in Japan. Plant Pathology, 59, 76–83. https://doi.org/10.1111/j.1365-3059.2009.02207.x

Kirkegaard, J. A., & Matthiessen, J. N. (2004). Developing and refining the biofumigation concept. Agroindustria, 3(3), 233–239.

León, L., Silverio, F., López, M. M., & Rodriguez, A. (2011). Clavibacter michiganensis subsp. michiganensis, a seedborne tomato pathogen: healthy seeds are still the goal. Plant Disease, 95(11), 1328–1338. https://doi.org/10.1094/PDIS-02-11-0091

Maeso, D., Arboleya, J., & Walasek, W. (2012). Supervivencia de Clavibacter michiganensis subsp. michiganensis, agente causal del “cancro bacteriano del tomate” en elementos de entutorado. Horticultura Argentina, 31(75), 28–31. https://www.horticulturaar.com.ar/es/publicacion/75/

Makane, M., Lehnhoff, E. A., Trainor, P. J., & Sanogo, S. (2023). Suppression of Phytophthora capsici in chile pepper using Brassica juncea and Hordeum vulgare cover crop residues and Trichoderma harzianum as a biocontrol agent. Plant Disease, 107(11), 3457–3463. https://doi.org/10.1094/PDIS-10-22-2485-RE

Malliarakis, D., Pagoulatou, M. G., Mpalantinaki, E., Trantas, E., Ververidis, F., & Goumas, D. E. (2023). Phylogenetic diversity of Clavibacter michiganensis subsp. michiganensis isolates causing bacterial canker of tomato in Greece. Journal of Plant Pathology, 105, 1403–1419. https://doi.org/10.1007/s42161-023-01375-4

Martin, F. N. (2003). Development of alternative strategies for management of soilborn pathogens currently controlled with methyl bromide. Annual Review of Phytopathology, 41, 325–350. https://doi.org/10.1146/annurev.phyto.41.052002.095514

Mitidieri, M. S., Piris, E., Brambilla, V., Barbieri, M., Cap, G., González, J., Del Pardo, K., Ciapone, M., Celié, R., Arpía, E., Paunero, I., Peralta, R., Verón, R., & Sánchez, F. (2015). Evaluación de parámetros de rendimiento y sanidad de dos híbridos comerciales de tomate (Solanum lycopersicum L.) injertados sobre Solanum sisymbriifolium (Lam.), en un invernadero con suelo biosolarizado. Horticultura Argentina, 34(84), 5–17. https://www.horticulturaar.com.ar/es/publicacion/84/

Morales-Rodríguez, C., Bastianelli, G., Aleandri, M. P., Chilosi, G., & Vannini, A. (2018). Application of Trichoderma spp. complex and biofumigation to control damping-off of Pinus radiata D. Don caused by Fusarium circinatum Nirenberg and O’Donnell. Forests, 9(7), Article 421. https://doi.org/10.3390/f9070421

Osdaghi, E. (2015). Clavibacter michiganensis (bacterial canker of tomato). Centre for Agricultural Bioscence International. CABI Digital Library. https://www.cabi.org/isc/datasheet/15338

Peñalba, J. (2022). Efecto de Trichoderma harzianum luego de una biofumigación para el biocontrol de Clavibacter michiganensis subsp. michiganensis en tomate [Undegraduate thesis, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata]. https://sedici.unlp.edu.ar/handle/10915/134048

Perniola, O. S., Staltari, S., Chorzempa, S. E., Astiz Gassó, M. M., & Molina, M. C. (2014). Control biológico de Fusarium graminearum: utilización de Trichoderma spp. y biofumigación con parte aérea de Brassica juncea. Revista de la Facultad de Ciencias Agrarias UN Cuyo, 46(2), 45–56. https://revistas.uncu.edu.ar/ojs3/index.php/RFCA/article/view/5603

Rolleri, J. (2015). Cancro bacteriano del tomate: diagnóstico y prevención de su dispersión en el cultivo [Master thesis, Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata]. https://doi.org/10.35537/10915/57635

Rolleri, J., & Romero, A. M. (2022). Prospección del marchitamiento y cancro bacteriano del tomate en invernaderos del Cinturón Hortícola Platense. Revista de Investigación Agropecuaria, 48(1), 104–110. https://www.redalyc.org/articulo.oa?id=86470768014

Rolleri, J., Stocco, M., Moya, P., & Mónaco, C. (2021). Posibilidades del uso de Trichoderma harzianum en el biocontrol del marchitamiento y cancro bacteriano del tomate. Revista de la Facultad de Agronomía, 120(2), 1–12. https://doi.org/10.24215/16699513e080

Sarandón, S., & Flores, C. (2014). Agroecología. Bases teóricas para el diseño y manejo de agroecosistemas sustentables. Editorial de la Universidad Nacional de La Plata (EDULP). DOI: https://doi.org/10.35537/10915/37280

Schaad, N. W., Jones, J. B., & Chun, W. (Eds.). (2001). Laboratory guide for identification of plant pathogenic bacteria (3rd ed.). St Paul, USA: American Phytopathological Society Press. https://doi.org/10.1046/j.1365-3059.2001.00635.x

Sood, M., Kappor, D., Kumar, B., Shetewiy, M. S., Ramakrishnan, M., Landi, M., Araniti, F., & Sharma, A. (2020). Trichoderma: The “secrets” of a multitalented biocontrol agent. Plants, 9(6), Article 762. https://doi.org/10.3390/plants9060762

Stocco, M., Lampugnani, G., Zuluaga, S., Abramoff, C., Cordo, C., & Mónaco, C. (2019). Fungicida biológico a base de una cepa del hongo Trichoderma harzianum: su supervivencia en el suelo. Revista de la Facultad de Agronomía, 118(2), Article 20. https://doi.org/10.24215/16699513e020

Stocco, M. C., Mónaco, C., Abramoff, C., Lampugnani, G., Salerno, G., Kripelz, N., Cordo, C., & Consolo, V. (2016). Selection and characterization of Argentine isolates of Trichoderma harzianum for effective biocontrol of Septoria leaf blotch of wheat. World Journal of Microbiology and Biotechnology, 32, Article 49. https://doi.org/10.1007/s11274-015-1989-9

Vega, D., & Romero, A. (2015). Survival of Clavibacter michiganensis subsp. michiganensis in tomato debris under greenhouse conditions. Plant Pathology, 65(4), 545–550. https://doi.org/10.1111/ppa.12444

Zahir, I., Babouchi, M., Boulanour, H., & El Louyti, M. (2018). Effet des microorganismes isolés á partir des biotipes Marocains sur les phytopatogénes: revue bibliographique. Agrobiologia, 8(2), 971–983. https://www.asjp.cerist.dz/en/article/119751

Zhang, D., Yan, D., Cheng, H., Fang, W., Huang, B., Wang, X., Wang, X., Yan, Y., Ouyang, C., Li, W., Wang, C., & Cao, A. (2020). Effects of multi-year biofumigation on soil bacterial and fungal communities and strawberry yield. Environmental Pollution, 256, Article 113415. https://doi.org/10.1016/j.envpol.2019.113415

How to Cite

APA

Stocco, M., Rolleri, J., Moya, P., Peñalba, J. & Mónaco, C. (2024). Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation. Agronomía Colombiana, 42(2), e114659. https://doi.org/10.15446/agron.colomb.v42n2.114659

ACM

[1]
Stocco, M., Rolleri, J., Moya, P., Peñalba, J. and Mónaco, C. 2024. Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation. Agronomía Colombiana. 42, 2 (May 2024), e114659. DOI:https://doi.org/10.15446/agron.colomb.v42n2.114659.

ACS

(1)
Stocco, M.; Rolleri, J.; Moya, P.; Peñalba, J.; Mónaco, C. Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation. Agron. Colomb. 2024, 42, e114659.

ABNT

STOCCO, M.; ROLLERI, J.; MOYA, P.; PEÑALBA, J.; MÓNACO, C. Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation. Agronomía Colombiana, [S. l.], v. 42, n. 2, p. e114659, 2024. DOI: 10.15446/agron.colomb.v42n2.114659. Disponível em: https://revistas.unal.edu.co/index.php/agrocol/article/view/114659. Acesso em: 27 dec. 2025.

Chicago

Stocco, Marina, Jorgelina Rolleri, Paulina Moya, Julieta Peñalba, and Cecilia Mónaco. 2024. “Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation”. Agronomía Colombiana 42 (2):e114659. https://doi.org/10.15446/agron.colomb.v42n2.114659.

Harvard

Stocco, M., Rolleri, J., Moya, P., Peñalba, J. and Mónaco, C. (2024) “Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation”, Agronomía Colombiana, 42(2), p. e114659. doi: 10.15446/agron.colomb.v42n2.114659.

IEEE

[1]
M. Stocco, J. Rolleri, P. Moya, J. Peñalba, and C. Mónaco, “Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation”, Agron. Colomb., vol. 42, no. 2, p. e114659, May 2024.

MLA

Stocco, M., J. Rolleri, P. Moya, J. Peñalba, and C. Mónaco. “Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation”. Agronomía Colombiana, vol. 42, no. 2, May 2024, p. e114659, doi:10.15446/agron.colomb.v42n2.114659.

Turabian

Stocco, Marina, Jorgelina Rolleri, Paulina Moya, Julieta Peñalba, and Cecilia Mónaco. “Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation”. Agronomía Colombiana 42, no. 2 (May 1, 2024): e114659. Accessed December 27, 2025. https://revistas.unal.edu.co/index.php/agrocol/article/view/114659.

Vancouver

1.
Stocco M, Rolleri J, Moya P, Peñalba J, Mónaco C. Preliminary findings on biocontrol of bacterial wilt and canker of tomato (Clavibacter michiganensis subsp. michiganensis) using Trichoderma harzianum after biofumigation. Agron. Colomb. [Internet]. 2024 May 1 [cited 2025 Dec. 27];42(2):e114659. Available from: https://revistas.unal.edu.co/index.php/agrocol/article/view/114659

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