Efecto de antibiosis, antixenosis y la variación natural de tricomas de especies silvestres y comerciales en tomate sobre el desarrollo de Bactericera cockerelli

Adela Nazareth García-Sánchez; Ernesto  Cerna Chávez; Mariana  Beltrán Beache; Yisa María  Ochoa Fuentes; Juan Carlos Delgado Ortiz

doi:10.17268/sci.agropecu.2023.041

Autores/as

Adela Nazareth García-Sánchez Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Coahuila, México. https://orcid.org/0009-0006-2453-5802
Ernesto Cerna Chávez Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Saltillo, Coahuila, México. https://orcid.org/0000-0003-2263-4322
Mariana Beltrán Beache Departamento de Agronomía, Universidad Autónoma de Aguascalientes, Aguascalientes, México. https://orcid.org/0000-0002-3109-9360
Yisa María Ochoa Fuentes Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Coahuila, México. https://orcid.org/0000-0001-7859-8434
Juan Carlos Delgado Ortiz Departamento de Parasitología, Universidad Autónoma Agraria Antonio Narro, Coahuila, México. https://orcid.org/0000-0003-4899-9995

DOI:

https://doi.org/10.17268/sci.agropecu.2023.041

Palabras clave:

Antixenosis, antibiosis, preferencia, resistencia, tomates silvestres, psílido del tomate

Resumen

Bactericera cockerelli es una plaga económicamente relevante para cultivos de solanáceas. La presencia de tricomas foliares con la que cuentan ciertas especies silvestres constituye importantes recursos genéticos para programas de fitomejoramiento en términos de resistencia a plagas. En este estudio se evaluó la influencia de los tricomas foliares de especies silvestres y cultivares comerciales de tomate en la preferencia, desarrollo y fecundidad de B. cockerelli. Los resultados mostraron que las especies silvestres fueron menos preferidas por el psílido que los cultivares comerciales. Los insectos mostraron un porcentaje de asentamiento menor en S. habrochaites en comparación con las demás especies. En cuanto a la supervivencia, el menor porcentaje se desarrolló en S. habrochaites con el 24% y S. arcanum con un 40%. La media de oviposición más baja se encontró en S. habrochaites con dos huevos, los cuales no eclosionaron, además, de ser la única especie que mostró la presencia de tricomas glandulares tipo IV (113,86 ± 48,1) y VIc (27,3 ± 2,3) por mm², asimismo su presencia se correlacionó negativamente con el número de adultos posados. S. arcanum fue otra especie que influyó negativamente en el comportamiento y desarrollo del insecto, sin embargo, estos atributos no fueron a causa de la presencia de tricomas. Los mecanismos de defensa manifestados por S. habrochaites y S. arcanum hacia B. cockerelli pueden ser utilizados como recurso de introgresión de genes para el manejo de esta plaga al reducir su potencial biológico.

Citas

Alba, J. M., Montserrat, M., & Fernández-Muñoz, R. (2009). Resistance to the two-spotted spider mite (Tetranychus urticae) by acylsucroses of wild tomato (Solanum pimpinellifolium) trichomes studied in a recombinant inbred line population. Exp. Appl. Acarol., 47, 35–47. https://doi.org/10.1007/s10493-008-9192-4

Almeida, K. C. de, Resende, J. T. V. de Hata, F. T., Oliveira, L. V. B., & Neto, J. G. (2023). Characterization of Solanum sp. Lycopersicon section for density and types of leaf trichomes and resistance to whitefly and tomato pinworm. Sci. Hortic. (Amsterdam), 310, 111746. https://doi.org/10.1016/j.scienta.2022.111746

Avila, C. A., Marconi, T. G., Viloria, Z., Kurpis, J., & Del Rio, S. Y. (2019). Bactericera cockerelli resistance in the wild tomato Solanum habrochaites is polygenic and influenced by the presence of Candidatus Liberibacter solanacearum. Sci. Reports, 9, 1–11. https://doi.org/10.1038/s41598-019-50379-7

Bai, Y., & Lindhout, P. (2007). Domestication and breeding of tomatoes: What have we gained and what can we gain in the future? Ann. Bot., 100, 1085–1094. https://doi.org/10.1093/aob/mcm150

Bleeker, P. M., Mirabella, R., Diergaarde, P. J., VanDoorn, A., Tissier, A., et al. (2012). Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc. Natl. Acad. Sci., 109, 20124–20129. https://doi.org/10.1073/PNAS.1208756109

Cerna-Chávez, E., Hernández-Bautista, O., Ochoa-Fuentes, Y. M., Landeros-Flores, J., Aguirre-Uribe, L. A., & Hernández-Juárez, A. (2018). Morphometric of immatures and life tables of Bactericera cockerelli (Hemiptera: Triozidae) from populations of Northeastern Mexico. Rev. Colomb. Entomol., 44, 53–60. https://doi.org/10.25100/socolen.v44i1.6543

Channarayappa, S. G., Muniyappa, V., & Frist, R. H. (1992). Resistance of Lycopersicon species to Bemisia tabaci, a tomato leaf curl virus vector. Can. J. Bot., 70, 2184–2192. https://doi.org/10.1139/b92-270

Dawood, M. H., & Snyder, J. C. (2020). The Alcohol and Epoxy Alcohol of Zingiberene, Produced in Trichomes of Wild Tomato, Are More Repellent to Spider Mites Than Zingiberene. Front. Plant Sci., 11, 1. https://doi.org/10.3389/fpls.2020.00035

de Oliveira, J. R. F., de Resende, J. T. V., Maluf, W. R., Lucini, T., de Lima Filho, R. B., de Lima, I. P., & Nardi, C. (2018). Trichomes and allelochemicals in tomato genotypes have antagonistic effects upon behavior and biology of tetranychus urticae. Front. Plant Sci., 9, 1132. https://doi.org/10.3389/fpls.2018.01132

Delgado-Ortiz, J. C., Beltrán-Beache, M., Cerna-Chávez, E., Aguirre-Uribe, L. A., Landero-Flores, J., Rodríguez-Pagaza, Y., & Ochoa-Fuentes, Y. M. (2019). Candidatus Liberibacter solanacearum patógeno vascular de solanáceas: Diagnóstico y control. TIP Rev. Espec. en Delgado-Ortiz, J. C. et al. Candidatus Lib. solanacearum patógeno Vasc. solanáceas Diagnó 22, 1–12. https://doi.org/10.22201/fesz.23958723e.2019.0.177

Eigenbrode, S. D., Trumble, J. T., & Jones, R. A. (2019). Resistance to Beet Armyworm, Hemipterans, and Liriomyza spp. in Lycopersicon Accessions. J. Am. Soc. Hortic. Sci., 118, 525–530. https://doi.org/10.21273/jashs.118.4.525

Fernández-Muñoz, R., Salinas, M., Álvarez, M., & Cuartero, J. (2003). Inheritance of resistance to two-spotted spider mite and glandular leaf trichomes in wild tomato Lycopersicon pimpinellifolium (Jusl.) Mill. J. Am. Soc. Hortic. Sci., 128, 188–195. https://doi.org/10.21273/jashs.128.2.0188

Garzón-Tiznado, J. A., Lugo-Lujan, J. M., Hernández-Verdugo, S., Medina-López, R., Velarde-Félix, S., Portillo-Loera, J. J., & Retes-Manjarrez, J. E. (2020). Antixenosis of Mexican Landrace and Wild Tomato Populations to Bemisia tabaci. Southwest. Entomol., 45, 501–510. https://doi.org/10.3958/059.045.0218

Heinz, K. M., & Zalom, F. G. (1995). Variation in Trichome-Based Resistance to Bemisia argentifolii (Homoptera: Aleyrodidae) Oviposition on Tomato. J. Econ. Entomol., 88, 1494–1502. https://doi.org/10.1093/JEE/88.5.1494

Jablonska, B., Ammiraju, J. S. S., Bhattarai, K. K., Mantelin, S., De Ilarduya, O. M., Roberts, P. A., & Kaloshian, I. (2007). The Mi-9 Gene from Solanum arcanum Conferring Heat-Stable Resistance to Root-Knot Nematodes Is a Homolog of Mi-1. Plant Physiol., 143, 1044–1054. https://doi.org/10.1104/PP.106.089615

Levy, J., Ravindran, A., Gross, D., Tamborindeguy, C., & Pierson, E. (2011). Translocation of “Candidatus Liberibacter solanacearum”, the Zebra Chip Pathogen in Potato and Tomato. Phytopathology, 101, 1285. https://doi.org/10.1094/PHYTO-04-11-0121

Liu, D., & Trumble, J. T. (2007). Comparative fitness of invasive and native populations of the potato psyllid (Bactericera cockerelli). Entomol. Exp. Appl., 123, 35–42. https://doi.org/10.1111/j.1570-7458.2007.00521.x

Luna-Cruz, A., Lomeli-Flores, J. R., Rodríguez-Leyva, E., Ortega-Arenas, L. D., & Huerta de La Peña, A. (2011). Toxicidad de cuatro insecticidas sobre Tamarixia triozae (Burks) (Hymenoptera: Eulophidae) y su hospedero Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). Acta zoológica mexicana, 27(3), 509-526.

Marchant, W. G., Legarrea, S., Smeda, J. R., Mutschler, M. A., & Srinivasan, R. (2020). Evaluating acylsugars-mediated resistance in tomato against Bemisia tabaci and transmission of tomato yellow leaf curl virus. Insects, 11, 842.

Mayo-Hernández, J., Ramírez-Chávez, E., Molina-Torres, J., Guillén-Cisneros, M.d.L., Rodríguez-Herrera, R., et al. (2019) Effects of Bactericera cockerelli Herbivory on Volatile Emissions of Three Varieties of Solanum lycopersicum. Plants, 8, 509. https://doi.org/10.3390/plants8110509

McDowell, E. T., Kapteyn, J., Schmidt, A., Li, C., Kang, J. H., et al. (2011). Comparative functional genomic analysis of solanum glandular trichome types. Plant Physiol., 155, 524–539. https://doi.org/10.1104/pp.110.167114

Moghe, G., Irfan, M., & Sarmah, B. (2023). Dangerous sugars: Structural diversity and functional significance of acylsugar-like defense compounds in flowering plants. Curr. Opin. Plant Biol., 73, 102348. https://doi.org/10.1016/J.PBI.2023.102348

Molki, B., Ha, P. T., Cohen, A. L., Crowder, D. W., Gang, D. R., Omsland, A., Brown, J. K., & Beyenal, H. (2019). The infection of its insect vector by bacterial plant pathogen “Candidatus Liberibacter solanacearum” is associated with altered vector physiology. Enzyme Microb. Technol., 129, 109358.

Mora, V., Ramasamy, M., Damaj, M. B., Irigoyen, S., Ancona, V., Avila, C. A., Vales, M. I., Ibanez, F., Mandadi, K. K. (2022). Identification and Characterization of Potato Zebra Chip Resistance Among Wild Solanum Species. Front Microbiol., 27(13), 857493. doi: 10.3389/fmicb.2022.857493

Nombela, G., Williamson, V. M., & Muñiz, M. (2003). The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant-Microbe Interact., 16, 645–649.

Olaniyan, O., Rodríguez-Gasol, N., Cayla, N., Michaud, E., & Wratten, S. D. (2020). Bactericera cockerelli (Sulc), a potential threat to China’s potato industry. J. Integr. Agric., 19, 338–349.

Panizzon, F. C., Vilela de Resende, J. T., Lima-Filho, R. B., de Pilati, L., Gomes, G. C., Roberto, S. R., & Da-Silva, P. R. (2022). Development of BC3F2 Tomato Genotypes with Arthropod Resistance Introgressed from Solanum habrochaites var. hirsutum (PI127826). Hortic., 8, 1217. https://doi.org/10.3390/HORTICULTURAE8121217

Paudel, S., Felton, G. W., & Rajotte, E. G. (2022). Anti-Herbivore Resistance Changes in Tomato with Elevation. J. Chem. Ecol., 48, 196–206. https://doi.org/10.1007/S10886-021-01341-3

Prager, S. M., & Trumble, J. T. (2018). Psyllids: Biology, Ecology, and Management. In Sustain. Manag. Arthropod Pests Tomato (Chapter 7): 163–181. https://doi.org/10.1016/B978-0-12-802441-6.00007-3

Rakha, M., Bouba, N., Ramasamy, S., Regnard, J. L., & Hanson, P. (2017). Evaluation of wild tomato accessions (Solanum spp.) for resistance to two-spotted spider mite (Tetranychus urticae Koch) based on trichome type and acylsugar content. Genet. Resour. Crop Evol., 64, 1011–1022. https://doi.org/10.1007/s10722-016-0421-0

Rodríguez-López, M. J., Moriones, E., Fernández-Muñoz, R. (2020) An Acylsucrose-Producing Tomato Line Derived from the Wild Species Solanum pimpinellifolium Decreases Fitness of the Whitefly Trialeurodes vaporariorum. Insects, 11, 616. https://doi.org/10.3390/insects11090616

Roque, A., Delgado-Ortiz, J. C., Beltrán-Beache, M., Ochoa-Fuentes, Y., & Cerna-Chávez, E. (2021). Parámetros agronómicos del tomate (Solanum lycopersicum L.) inoculado con “Candidatus Liberibacter solanacearum” y tratados con fosfitos. Ecosistemas y Recur. Agropecu. 8. https://doi.org/10.19136/era.a8n1.2552

Rossi, M., Goggin, F. L., Milligan, S. B., Kaloshian, I., Ullman, D. E., & Williamson, V. M. (1998). The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl. Acad. Sci., 95, 9750–9754. https://doi.org/10.1073/pnas.95.17.9750

Sánchez-Peña, P., Oyama, K., Núñez-Farfán, J., Fornoni, J., Hernández-Verdugo, S., Márquez-Guzmán, J., & Garzón-Tiznado, J. A. (2006). Sources of resistance to whitefly (Bemisia spp.) in wild populations of Solanum lycopersicum var. cerasiforme (Dunal) spooner G.J. Anderson et R.K. Jansen in Northwestern Mexico. Genet. Resour. Crop Evol., 53, 711–719. https://doi.org/10.1007/s10722-004-3943-9

Savi, P. J., Moraes, G. J. D., Junior, A. L. B., Melville, C. C., Carvalho, R. F., Lourenção, A. L., & Andrade, D. J. (2019). Impact of leaflet trichomes on settlement and oviposition of Tetranychus evansi (Acari: Tetranychidae) in African and South American tomatoes. Syst. Appl. Acarol., 24, 2559–2576.

Szczepaniec, A., Varela, K. A., Kiani, M., Paetzold, L., & Rush, C. M. (2019). Incidence of resistance to neonicotinoid insecticides in Bactericera cockerelli across Southwest U.S. Crop Prot., 116, 188–195. https://doi.org/10.1016/j.cropro.2018.11.001

Thomas, K. L., Jones, D. C., Kumarasinghe, L. B., Richmond, J. E., Gill, G. S. C., & Bullians, M. S. (2011). Investigation into the entry pathway for tomato potato psyllid Bactericera cockerelli. New Zeal. Plant Prot., 64, 259–268. https://doi.org/10.30843/nzpp.2011.64.6008

Vargas-Madríz, H., Bautista-Martínez, N., Vera-Graziano, J., García-Gutiérrez, C., & Chavarín-Palacio, C. (2013). Morphometrics of Eggs, Nymphs, and Adults of Bactericera cockerelli (Hemiptera: Triozidae), Grown on Two Varieties of Tomato Under Greenhouse Conditions. Florida Entomologist, 96(1), 71-79. https://doi.org/10.1653/024.096.0110

Vereijssen, J. (2020). Ecology and management of Bactericera cockerelli and Candidatus Liberibacter solanacearum in New Zealand. J. Integr. Agric., 19, 333–337. https://doi.org/10.1016/S2095-3119(19)62641-9

Walker, P. W., Allen, G. R., Tegg, R. S., White, L. R., & Wilson, C. R. (2015). The tomato potato psyllid, Bactericera cockerelli (Šulc, 1909) (Hemiptera: Triozidae): A review of the threat of the psyllid to Australian solanaceous crop industries and surveillance for incursions in potato crops. Austral Entomol., 54, 339–349. https://doi.org/10.1111/AEN.12129

Wang, F., Park, Y. L., & Gutensohn, M. (2021). Epidermis-Specific Metabolic Engineering of Sesquiterpene Formation in Tomato Affects the Performance of Potato Aphid Macrosiphum euphorbiae. Front. Plant Sci., 12, 3052. https://doi.org/10.3389/FPLS.2021.793313

Workneh, F., Trees, J. L., Paetzold, L., Badillo-Vargas, I. E., & Rush, C. M. (2020). Impact of ‘Candidatus Liberibacter solanacearum’ haplotypes on sprout emergence and growth from infected seed tubers. Crop Prot., 105462. https://doi.org/10.1016/j.cropro.2020.105462

Yang, X. B., & Liu, T. X. (2009). Life history and life tables of bactericera cockerelli (Homoptera: Psyllidae) on eggplant and bell pepper. Environ. Entomol., 38, 1661–1667. https://doi.org/10.1603/022.038.0619

Yang, X. B., Zhang, Y. M., Hua, L., & Liu, T. X. (2010). Life history and life tables of Bactericera cockerelli (Hemiptera: Psyllidae) on potato under laboratory and field conditions in the Lower Rio Grande Valley of Texas. J. Econ. Entomol., 103, 1729–1734. https://doi.org/10.1603/EC10083