Molecular aspects of tomato (Solanum lycopersicum) vascular wilt by Fusarium oxysporum f. sp. lycopersici and antagonism by Trichoderma spp.

Paula Andrea Castillo-Sanmiguel, Laura Rocío Cortés-Sánchez, Jovanna Acero-Godoy

Abstract


Tomato plants (Solanum lycopersicum) are susceptible to the infection by diverse pathogens that cause devastating diseases such as vascular wilt, which causes great losses at the production level. The fungus Fusarium oxysporum f. sp. lycopersici (Fol) is one of the etiologic agents of this disease and its control lies in the use of synthetic chemicals which generate a negative impact in both health and the environment; thus, it is necessary to implement biological control as a healthier and more efficient alternative. The fungus Trichoderma spp. is a favorable option to be employed as a biocontroller against this pathogen thanks to its antagonist mechanisms, determined by metabolic and genetic characteristics. On the one hand, for Fol it is indispensable the activation of signaling routes such as MAPK Fmk1, MAPK Mpk1 y HOG, while Trichoderma spp. uses effectors involved in the interaction with the plant such as proteins, enzymes and secondary metabolites that also strengthen its immune response against infection, determined by both Pathogen Associated Molecular Patterns (PAMP) and effectors. Therefore, this article makes a review about the mentioned characteristics and suggests a greater application of tools and molecular markers for the management of this disease.


Keywords


vascular wilt; Fusarium oxysporum f. sp. lycopersici; biological control; Trichoderma spp.

Full Text:

PDF

References


Aamir M, Singh V, Dubey M, Kashyap S, Zehra A, Upadhyay R and Singh S. 2018. Structural and functional dissection of differentially expressed tomato WRKY transcripts in host defense response against the vascular wilt pathogen (Fusarium oxysporum f. sp. lycopersici). PLoS One 13(4): 1-43. https://doi.org/10.1371/journal.pone.0193922

Aamir M, Kashyap S, Zehra A, Dubey M, Singh V, Ansari W, Upadhyay R and Singh S. 2019. Trichoderma erinaceum bio-priming modulates the WRKYs defense programming in tomato against the Fusarium oxysporum f. sp. lycopersici (Fol) challenged condition. Frontiers in Plant Science 10(911): 1-21. https://doi.org/10.3389/fpls.2019.00911

Alfiky A and Weisskopf L. 2021. Deciphering Trichoderma–plant–pathogen interactions for better development of biocontrol applications. Journal of Fungi 7(1): 61. https://doi.org/10.3390/jof7010061

Andrade-Hoyos P, Molina E, De León C, Espíndola M, Alvarado D y López A. 2015. Mecanismos de defensa en portainjertos de aguacate ante Phytophthora cinnamomi Rands. Revista Mexicana de Ciencias Agrícolas 6(2): 347-360. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S2007-09342015000200010

Bai Y, Sunarti S, Kissoudis C, Visser R and Van der Linden C. 2018. The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses. Frontiers in Plant Science 9(801): 1-7. https://doi.org/10.3389/fpls.2018.00801

Burbano E and Vallejo F. 2017. Production of “chonto” tomato lines, Solanum lycopersicum Mill., with expression of the sp gene responsible of determinate growth. Revista Colombiana de Ciencias Hortícolas 11(1): 63-71. http://dx.doi.org/10.17584/rcch.2017v11i1.5786

Cardona-Piedrahita L y Castaño-Zapata J. 2019. Comparación de métodos de inoculación de Fusarium oxysporum f. sp. lycopersici, causante del marchitamiento vascular del tomate. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 43(167): 227-233. http://dx.doi.org/10.18257/raccefyn.854

Carmona S, Burbano-David D, Gómez M, Lopez W, Ceballos N, Castaño-Zapata J, Simbaqueba J and Soto-Suárez M. 2020. Characterization of pathogenic and nonpathogenic Fusarium oxysporum isolates associated with commercial tomato crops in the andean region of Colombia. Pathogens 9(70): 1-23. https://doi.org/10.3390/pathogens9010070

Córdova-Albores L, Zelaya-Molina L, Ávila-Alistac N, Valenzuela-Ruíz V, Cortés-Martinez N, Parra-Cota F, Burgos-Canul Y, Chávez-Díaz I, Fajardo-Franco M and Santos-Villalobos S. 2021. Omics sciences potential on bioprospecting of biological control microbial agents: the case of the Mexican agro-biotechnology. Mexican Journal of Phytopathology 39(1): 147-184. https://doi.org/10.18781/r.mex.fit.2009-3

Cruz M, Hoyos L y Melgarejo L. 2012. Respuesta fisiológica de la gulupa (Passiflora edulis) frente al ataque por Fusarium spp. Universidad Nacional de Colombia 5(1): 91-112. https://repositorio.unal.edu.co/bitstream/handle/unal/11145/07_Cap05.pdf?sequence=2&isAllowed=y

Cubillos J, Páez A y Mejía L. 2011. Evaluación de la capacidad biocontroladora de Trichoderma harzianum Rifai contra Fusarium solani (Mart.) Sacc. asociado al complejo “secadera” en maracuyá, bajo condiciones de invernadero. Revista Facultad Nacional de Agronomía Medellín 64(1): 5821-5830. https://www.redalyc.org/articulo.oa?id=179922364008

De Sain M and Rep M. 2015. The role of pathogen-secreted proteins in fungal vascular wilt diseases. International Journal of Molecular Sciences 16(10): 23970-23993. https://doi.org/10.3390/ijms161023970

Domínguez S, Rubio M, Cardoza R, Gutiérrez S, Nicolás C, Bettiol W, Hermosa R and Monte E. 2016. Nitrogen metabolism and growth enhancement in tomato plants challenged with Trichoderma harzianum expressing the Aspergillus nidulans acetamidase amdS gene. Frontiers in Microbiology 7(1182): 1-14. https://doi.org/10.3389/fmicb.2016.01182

Eraso C, Acosta J, Salazar C y Betancourth C. 2014. Evaluación de cepas de Trichoderma spp. para el manejo del amarillamiento de arveja causado por Fusarium oxysporum. Revista Ciencia & Tecnología Agropecuaria 15(2): 237-249. https://doi.org/10.21930/rcta.vol15_num2_art:363

Florido M y Álvarez M. 2015. Aspectos relacionados con el estrés de calor en tomate (Solanum lycopersicum L.). Revista Cultivos Tropicales 36(1): 77-95. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0258-59362015000500008

García-Enciso E, Benavidez-Mendoza A, Flores-López M, Robledo-Olivo A, Juárez-Maldonado A and González-Morales S. 2017. A molecular vision of the interaction of tomato plants and Fusarium oxysporum f. sp. lycopersici. IntechOpen 6(1): 80-99. http://dx.doi.org/10.5772/intechopen.72127

Gawehns F, Ma L, Bruning O, Houterman P, Boeren S, Cornelissen B, Rep M and Takken F. 2015. The effector repertoire of Fusarium oxysporum determines the tomato xylem proteome composition following infection. Frontiers in Plant Science 6(967): 1-17. https://doi.org/10.3389/fpls.2015.00967

Gonzalez-Cendales Y, Catanzarit A, Baker B, Mcgrath D and Jones DA. 2015. Identification ofI-7expands the repertoire of genes for resistance to Fusarium wilt in tomato to three resistance gene classes. Molecular Plant Pathology 17(3): 448-463. https://doi.org/10.1111/mpp.12294

González I, Arias Y y Peteira B. 2012. Aspectos generales de la interacción Fusarium oxysporum f. sp. lycopersici-tomate. Revista Protección Vegetal 27(1): 1-7. http://scielo.sld.cu/pdf/rpv/v27n1/rpv01112.pdf

González-López M, Jijón-Moreno S, Dautt-Castro M, Ovando-Vásquez C, Ziv T, Horwitz B and Casas-Flores S. 2021. Secretome analysis of Arabidopsis–Trichoderma atroviride interaction unveils new roles for the plant glutamate: glyoxylate aminotransferase GGAT1 in plant growth induced by the fungus and resistance against Botrytis cinerea. International Journal of Molecular Sciences 22(13): 6804. https://doi.org/10.3390/ijms22136804

Guzmán-Guzmán P, Alemán-Duarte M, Delaye L, Herrera-Estrella A and Olmedo-Monfil V. 2017. Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genomics 18(16): 1-20. https://doi.org/10.1186/s12863-017-0481-y

Henao-Henao E, Hernández-Medina C, Salazar-González C, Velasco-Belalcazar M and Gómez-López E. 2018. Molecular identification of Fusarium isolates associated with passion fruit in five locations from Valle del Cauca, Colombia. Mesoamerican Journal of Agronomy 29(1): 53-61. https://doi.org/10.15517/ma.v29i1.27114

Hernández-Melchor D, Ferrera-Cerrato R y Alarcón A. 2019. Trichoderma: Importancia agrícola, biotecnológica, y sistemas de fermentación para producir biomasa y enzimas de interés industrial. Chilean Journal of Agricultural & Animal Sciences 35(1): 98-112. http://dx.doi.org/10.4067/S0719-38902019005000205

Herrera-Téllez V, Cruz-Olmedo A, Plasencia J, Gavilanes-Ruíz M, Arce-Cervantes O, Hernández-León S and Saucedo-García M. 2019. The protective effect of Trichoderma asperellum on tomato plants against Fusarium oxysporum and Botrytis cinerea diseases involves inhibition of reactive oxygen species production. International Journal of Molecular Sciences 20(8): 1-13. https://doi.org/10.3390/ijms20082007

Hu Z, Parekh U, Maruta N, Trusov Y and Botella J. 2015. Down-regulation of Fusarium oxysporum endogenous genes by host-delivered RNA interference enhances disease resistance. Frontiers in Chemistry 3(1): 1-10. https://doi.org/10.3389/fchem.2015.00001

Jaroszuk-?cise? J, Ty?kiewicz R, Nowak A, Ozimek E, Majewska M, Hanaka A, Ty?kiewicz K, Pawlik A and Janusz G. 2019. Phytohormones (auxin, gibberellin) and ACC deaminase in vitro synthesized by the mycoparasitic Trichoderma DEMTKZ3A0 strain and changes in the level of auxin and plant resistance markers in wheat seedlings inoculated with this strain conidia. International Journal of Molecular Sciences 20(19): 4923. https://doi.org/10.3390/ijms20194923

Khan R, Najeeb S, Hussain S, Xie B and Li Y. 2020. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms 8(6): 817. https://doi.org/10.3390/microorganisms8060817

Kubicek C, Steindorff A, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy A, Kubicek E, Kuo A, Baroncelli R, Sarrocco S, Ferreira E, Vannacci G, Shen Q, Grigoriev I and Druzhinina I. 2019. Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20(485): 1-24. https://doi.org/10.1186/s12864-019-5680-7

Li C, Zuo C, Deng G, Kuang R, Yang Q, Hu C, Sheng O, Zhang S, Ma L, Wei Y, Yang J, Liu S, Biswas M, Viljoen A and Yi G. 2013. Contamination of bananas with bauvericin and fusaric acid produced by Fusarium oxysporum f. sp. cubense. PLoS One 8(7): 1-11. https://doi.org/10.1371/journal.pone.0070226

Matarese F, Sarrocco S, Gruber S, Seidl-Seiboth V and Vanacci G. 2012. Biocontrol of Fusarium head blight: interactions between Trichoderma and mycotoxigenic Fusarium. Microbiology Society Journal 158(1): 99-101. https://doi.org/10.1099/mic.0.052639-0

Manikandan R, Harish S, Karthikeyan G and Raguchander T. 2018. Comparative proteomic analysis of different isolates of Fusarium oxysporum f.sp. lycopersici to exploit the differentially expressed proteins responsible for virulence on tomato plants. Frontiers in Microbiology 9(420): 1-13. https://doi.org/10.3389/fmicb.2018.00420

Manganiello G, Sacco A, Ercolano MR, Vinale F, Lanzuise S, Pascale A, Napolitano M, Lombardi N, Lorito M and Woo S. 2018. Modulation of tomato response to Rhizoctonia solani by Trichoderma harzianum and its secondary metabolite harzianic acid. Frontiers in Microbiology 9(1966): 1-15. https://doi.org/10.3389/fmicb.2018.01966

Martínez B, Infante D y Reyes Y. 2013. Trichoderma spp. y su función en el control de plagas en los cultivos. Revista de Protección Vegetal 28(1): 1-11. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S1010-27522013000100001

Miranda D, Fischer G, Barrientos J, Carranza C, Rodríguez M and Lanchero J. 2009. Characterization of productive systems of tomato (Solanum lycopersicum) in producing zones of Colombia. Acta Horticulturae 821(821): 35-46. https://doi.org/10.17660/ActaHortic.2009.821.2

Mohanta T, Park Y and Bae H. 2016. Novel genomic and evolutionary insight of WRKY transcription factors in plant lineage. Scientific Reports 6(37309): 1-19. https://doi.org/10.1038/srep37309

Mukherjee P, Horwitz B and Kenerley C. 2012. Secondary metabolism in Trichoderma - a genomic perspective. Microbiology Society Journal 158(1): 35-45. https://doi.org/10.1099/mic.0.053629-0

Nusaibah S and Musa H. 2019. A review report on the mechanism of Trichoderma spp. as biological control agent of the basal stem rot (BSR) disease of Elaeis guineensis. IntechOpen 6(1): 1-12. https://doi.org/10.5772/intechopen.84469

Ojha S and Chatterjee N. 2011. Mycoparasitism of Trichoderma spp. in biocontrol of fusarial wilt of tomato. Archives of Phytopathology and Plant Protection 44(8): 771-782. https://doi.org/10.1080/03235400903187444

Okungbowa F and Shittu H. 2012. Fusarium wilts: an overview. Environmental Research Journal 6(2): 83-102. https://www.researchgate.net/profile/Hakeem-Shittu/publication/292243135_Fusarium_Wilts_An_Overview/links/56b252c908ae795dd5c7b24f/Fusarium-Wilts-An-Overview.pdf

Padilla-Ramos R, Salas-Muñoz S, Velázques-Valle R and Reveles-Torres L. 2021. A novel molecular approach in the study of parasite-host interaction. Mexican Journal of Phytopathology 37(1): 95-114. https://doi.org/10.18781/r.mex.fit.1808-6

Pérez-Almeida I, Morales-Astudillo R, Medina-Litardo R, Salcedo-Rosales G, Dascon A y Solano-Castillo T. 2016. Evaluación molecular de genotipos de tomate por su resistencia a Meloidogyne incognita, Fusarium oxysporum y Ralstonia solanacearum con fines de mejoramiento. Revista Bioagro 28(2): 107-116. http://www.ucla.edu.ve/bioagro/Rev28%282%29/5.%20ms%201540.pdf

Petit-Houdenot Y and Fudal I. 2017. Complex interactions between fungal avirulence genes and their corresponding plant resistance genes and consequences for disease resistance management. Frontiers in Plant Science 8(1072): 1-8. https://doi.org/10.3389/fpls.2017.01072

Poveda J, Abril-Urias P and Escobar C. 2020. Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Frontiers in Microbiology 11(992): 1-14. https://doi.org/10.3389/fmicb.2020.00992

Ramírez-Valdespino C, Casas-Flores S and Olmedo-Monfil V. 2019. Trichoderma as a model to study effector-like molecules. Frontiers In Microbiology 10(1030): 1-14. https://doi.org/10.3389/fmicb.2019.01030

Rodríguez-Cabello J, Pérez-González A, Ortega-García L y Arteaga-Barrueta M. 2020. Estudio hidrosostenible en el cultivo del tomate, su efecto en el rendimiento y calidad del fruto. Cultivos Tropicales 41(2): 1-15. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0258-59362020000200006&lng=es&nrm=iso

De Miguel-Rojas C. 2014. Papel de los reguladores moleculares Fbp1 y Bmh2 en la virulencia de Fusarium oxysporum. Departamento de genética de la Universidad de Córdoba. https://helvia.uco.es/xmlui/bitstream/handle/10396/12019/2014000000949.pdf?sequence=1

Ronnie-Gakegne E y Martínez-Coca B. 2018. Antibiosis y efecto de pH-temperatura sobre el antagonismo de cepas de Trichoderma asperellum frente a Alternaria solani. Revista de Protección Vegetal 33(2): 1-9. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S1010-27522018000200008&lng=es&nrm=iso&tlng=es#B7

Sánchez-Espinosa A, Villarruel-Ordaz J and Maldonado-Bonilla L. 2020. The cause and potential solution to the Fusarium wilt disease in banana plants. Terra Latinoamericana 38(2): 435-442. https://doi.org/10.28940/terra.v38i2.617

Sharma I and Sharma A. 2020. Trichoderma–Fusarium interactions: A biocontrol strategy to manage wilt. Pp: 167-185. In: Sharma A and Sharma P (eds.). Trichoderma: Host pathogen interactions and applications. USA. 331p

Sharma L and Marques G. 2018. Fusarium, an entomopathogen-a myth or reality? Pathogens 7(4): 1-15. https://doi.org/10.3390/pathogens7040093

Silva R, Neves V, Stecca A, Vieira E, Ferreira E and Ulhoa C. 2019. Trichoderma/pathogen/plant interaction in pre-harvest food security. Fungal Biology 123(8): 565-583. https://doi.org/10.1016/j.funbio.2019.06.010

Sonkar P, 2019. Determination of interaction between Trichoderma asperellum and Fusarium oxysporum sp. by digital light microscopy and confocal microscopy. Journal of Microbial & Biochemical Technology 11(1): 1-4. https://doi.org/10.4172/1948-5948.1000407

Sood M, Kapoor D, Kumar D, Sheteiwy M, Ramakrishnan M, Landi M, Araniti, F and Sharma A. 2020. Trichoderma: the “secrets” of a multitalented biocontrol agent. Plants 9(6): 1-25. https://doi.org/10.3390/plants9060762

Srinivas C, Nirmala D, Narasimha K, Dhananjaya C, Lakshmeesha T, Singh B, Kumar N, Niranjana S, Hashem A, Alqarawi A, Tabassum B, Fathy E, Nayaka C and Srivastava R. 2019. Fusarium oxysporum f. sp. lycopersici causal agent of vascular wilt disease of tomato: biology to diversity-a review. Saudi Journal of Biological Sciences 26(7): 1315-1324. https://doi.org/10.1016/j.sjbs.2019.06.002

Thrall P, Barrett L, Doods P and Burdon J. 2016. Epidemiological and evolutionary outcomes in gene-for-gene and matching allele models. Frontiers in Plant Science 6(1084): 1-12. https://doi.org/10.3389/fpls.2015.01084

Vargas-Hoyos H y Gilchrist-Ramelli E. 2015. Producción de enzimas hidrolíticas y actividad antagónica de Trichoderma asperellum sobre dos cepas de Fusarium aisladas de cultivos de tomate (Solanum lycopersicum). Revista Mexicana de Micología 42(1): 9-16. http://www.scielo.org.mx/scielo.php?pid=S0187-31802015000200003&script=sci_arttext

Villa-Martínez A, Pérez-Leal R, Morales-Morales H, Basurto-Sotelo M, Soto-Parra J y Martínez-Escudero E. 2014. Situación actual en el control de Fusarium spp. y evaluación de la actividad antifúngica de extractos vegetales. Acta Agronómica 64(2): 194-205. http://dx.doi.org/10.15446/acag.v64n2.43358

Vos C, De Cremer K, Cammue B and De Coninck B. 2015. The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease. Molecular Plant Pathology 16(4): 400-412. https://doi.org/10.1111/mpp.12189

Wu Q, Sun R, Ni M, Yu J, Li Y, Yu C, Dou K, Ren J and Chen J. 2017. Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLoS One 12(6): 1-20. https://doi.org/10.1371/journal.pone.0179957




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.2106-1

Refbacks

  • There are currently no refbacks.