European Journal of Plant Pathology

, Volume 140, Issue 2, pp 385–397 | Cite as

Effect of metabolites from different Trichoderma strains on the growth of Rosellinia necatrix, the causal agent of avocado white root rot

  • I. Arjona-Girona
  • F. Vinale
  • D. Ruano-Rosa
  • M. Lorito
  • C. J. López-Herrera


Seven different strains of Trichoderma isolated from avocado roots showed antagonism to Rosellinia necatrix, which is the causal agent of white root rot. We studied these Trichoderma strains on the basis of the secondary metabolites produced in liquid culture. Five different compounds, namely, 6PP (6-pentyl-α-pyrone), Harzianolide (4-hexa-2,4-dienyl-3-(2-hydroxy-propyl)-5H-furan-2-one), T39butenolide (4-hexa-2,4-dienyl-3-(2-oxo-propyl)-5H-furan-2-one), Dehydroharzianolide (4-hexa-2,4-dienyl-3-propenyl-5H-furan-2-one) and Cerinolactone [(3-hydroxy-5-(6-isopropyl-3-methylene-3, 4, 4a, 5, 6, 7, 8, 8a-octahydronaphthalen-2-yl) dihydrofuran-2-one); a recently discovered novel metabolite], were obtained. In vitro studies of the effects of these compounds on different R. necatrix strains isolated from avocado roots and with different virulence demonstrated that 6PP had the strongest effect even at a low concentration. Although unstable, Cerinolactone and T39butenolide also had large effects on R. necatrix, mainly at a concentration of 200 μg. Harzianolide and Dehydroharzianolide exhibited the lowest effects on the pathogen. In vivo studies of Trichoderma metabolites on Lupinus luteus plants demonstrated the delay of white root rot epidemic through preventive application of 6PP or Harzianolide to seeds or plantlets by immersion in solutions of these metabolites at 1 mg l−1 (minimum effective dosage). In contrast, Cerinolactone only was effective at 10 mg l−1 when applied by plantlet immersion. Thus, this study reports the role that these metabolites could play for controlling avocado white root rot caused by R. necatrix.


Antagonistic fungi Antifungal assays Biocontrol Soil-borne fungi Volatile compounds 



This work was supported by the CICE-Junta de Andalucía grant (Grupo PAIDI, AGR-235) and by the Spanish Plan Nacional I + D + I from Ministerio de Ciencia e Innovación (Grant AGL 2008-05453-C02-02/AGR and AGL 2011-030354-CO2-02). In addition, this research was co-financed by FEDER funds (EU). The authors thank M. de Juan Santolalla for her help in the fungal filtrate extractions.

Supplementary material

10658_2014_472_MOESM1_ESM.pdf (1.8 mb)
ESM 1 (PDF 1856 kb)


  1. Almassi, F., Ghisalberti, E. L., Narbey, M., & Sivasisthamparan, K. (1991). New antibiotics from strains of Trichoderma harzianum. Journal of Natural Products, 54, 396–402.CrossRefGoogle Scholar
  2. Claydon, N., Allan, M., Hanson, J. R., & Avent, A. G. (1987). Antifungal alkyl pyrones of Trichoderma harzianum. Transactions of the British Mycological Society, 88, 503–513.CrossRefGoogle Scholar
  3. Cleland, R. (1972). The dosage-response curve for auxin-induced cell elongation: a re-evaluation. Planta, 104, 1–9.PubMedCrossRefGoogle Scholar
  4. Collins, R. P., & Halim, A. F. (1972). Characterization of the major aroma constituent of the fungus Trichoderma viride (Pers.). Journal of Agriculture Food Chemistry, 20, 437–438.CrossRefGoogle Scholar
  5. Contreras-Cornejo, H. A., Macias-Rodriguez, L., Cortes-Penagos, C., & Lopez-Bucio, J. (2009). Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiology, 149, 1579–92.PubMedCentralPubMedCrossRefGoogle Scholar
  6. Dunlop, R. W., Simon, A., Sivasisthamparan, K., & Ghisalberti, E. L. (1989). An antibiotic from Trichoderma koningii active against soil-borne plant pathogens. Journal of Natural Products, 52, 67–74.CrossRefGoogle Scholar
  7. El-Hassan, A., & Buchenauer, H. (2009). Actions of 6-pentyl-alpha-pyrone in controlling seedling blight incited by Fusarium moniliforme and inducing defence responses in maize. Journal of Phytopatology, 157, 697–707.CrossRefGoogle Scholar
  8. El-Hassan, A., Walker, F., Schöne, J., & Buchenauer, H. (2009). Detection of viridiofugin a and other antifungal metabolites excreted by Trichoderma harzianum active against different plant pathogens. European Journal of Plant Pathology, 124, 457–470.CrossRefGoogle Scholar
  9. Fernández-Escobar, R., Trapero, A., Domínguez, J. (2010). Experimentación en Agricultura. (Ed) Consejería de Agricultura y Pesca. Junta de Andalucía. p 350.Google Scholar
  10. Ghisalberti, E. L., Narbey, M. J., Dewan, M. M., & Sivasithamparam, K. (1990). Variability among strains of Trichoderma harzianum in their ability to reduce take-all and to produce pyrones. Plant and Soil, 121, 287–291.CrossRefGoogle Scholar
  11. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., & Lorito, M. (2004). Trichoderma species opportunistic, avirulent plant symbionts. Nature Reviews of Microbiology, 2, 43–56.CrossRefGoogle Scholar
  12. Hjeljord, L., Tronsmo, A. (1998). Trichoderma and Gliocladium biological control: an overwiew: Trichoderma and Gliocladium. Basic biology, taxonomy and genetics. In C. P. Kubicek G. E. Harman (Eds.). Taylor and Francis Ltd. (pp. 131–152).Google Scholar
  13. Howell C. R (1998). The role of antibiosis in biocontrol: Trichoderma and Gliocladium. Basic biology, taxonomy and genetics. In C. P. Kubicek, Harman G. E. (eds.) Taylor and Francis Ltd. (pp. 173–184).Google Scholar
  14. López Herrera, C.J (1998). Hongos de suelo en el cultivo del aguacate del litoral andaluz. V Jornadas Andaluzas de Frutos Tropicales (pp. 139–152).Google Scholar
  15. López Herrera, C. J., & Zea Bonilla, T. (2007). Effects of benomyl, carbendazim, fluazinam and thiophanate methyl on white root rot of avocado. Crop Protection, 26, 1186–1192.CrossRefGoogle Scholar
  16. López, M., Ruano Rosa, D., López Herrera, C. J., Monte, E., & Hermosa, R. (2008). Intraspecific diversity within avocado field isolates of Rosellinia necatrix from south-east Spain. European Journal of Plant Pathology, 121, 201–205.CrossRefGoogle Scholar
  17. Ruano Rosa, D., & López Herrera, C. J. (2009). Evaluation of Trichoderma spp. as biocontrol agents against avocado white root rot. Biological Control, 51, 66–71.CrossRefGoogle Scholar
  18. Ruano Rosa, D., del Moral Navarrete, L., & Lopez Herrera, C. J. (2010). Selection of Trichoderma spp. isolates antagonistic to Rosellinia necatrix. Spanish Journal of Agriculture Research, 8, 1084–1097.CrossRefGoogle Scholar
  19. Steel, R. G. D., & Torrie, J. H. (1985). Bioestadística: principios y procedimientos, 1ª ed en español (p. 622). Interamericana de México: McGraw-Hill.Google Scholar
  20. Uetake, Y., Nakamura, H., Arakawa, M., Okabe, I., & Matsumoto, N. (2001). Inoculation of lupinus luteus with white root rot fungus, Rosellinia necatrix, to estimate virulence. Journal of Genetic Plant Pathology, 67, 285–287.Google Scholar
  21. Vargas, W. A., Mandawe, J. C., & Kenerley, C. M. (2009). Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiology, 151, 792–808.PubMedCentralPubMedCrossRefGoogle Scholar
  22. Vargas, W. A., Crutcher, F. K., & Kenerley, C. M. (2011). Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association withplants by sucrose metabolism inside the fungal cells. New Phytology, 189, 777–89.CrossRefGoogle Scholar
  23. Vinale, F., Marra, R., Scala, F., Ghisalberti, E. L., Lorito, M., & Sivasithamparam, K. (2006). Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Letters on Applied Microbiology, 43, 143–148.CrossRefGoogle Scholar
  24. Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Barbetti, M. J., Li, H., Woo, S., & Lorito, M. (2008a). A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiology and Molecular Plant Pathology, 72, 80–86.CrossRefGoogle Scholar
  25. Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Woo, S. L., & Lorito, M. (2008b). Trichoderma–plant–pathogen interactions. Soil Biology Biochemistry, 40, 1–10.CrossRefGoogle Scholar
  26. Vinale, F., Ghisalberti, E. L., Sivasithamparam, K., Marra, R., Ritieni, A., Ferracane, R., Woo, S., & Lorito, M. (2009). Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters on Applied Microbiology, 48, 705–711.Google Scholar
  27. Vinale, F., Arjona Girona, I., Nigro, M., Mazzei, P., Piccolo, A., Ruocco, M., Woo, S., Ruano Rosa, D., López Herrera, C. J., & Lorito, M. (2012a). Cerinolactone, a hydroxy-lactone derivative from Trichoderma cerinum. Journal of Natural Products, 75, 103–106.Google Scholar
  28. Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Ruocco, M., Woo, S., & Lorito, M. (2012b). Trichoderma secondary metabolites that affect plant metabolism. Natural Products Communications, 7(11), 1545–1550.Google Scholar
  29. Zentmyer, G. A. (1984). Avocado diseases. Trop Pest Management, 30, 388–400.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2014

Authors and Affiliations

  • I. Arjona-Girona
    • 1
  • F. Vinale
    • 2
  • D. Ruano-Rosa
    • 1
  • M. Lorito
    • 3
  • C. J. López-Herrera
    • 1
  1. 1.Instituto de Agricultura Sostenible CSICCordobaSpain
  2. 2.CNR – Istituto per la Protezionedelle Piante (IPP-CNR)PorticiItaly
  3. 3.Dipartimento di AgrariaUniversità degli Studi di Napoli ‘Federico II’PorticiItaly

Personalised recommendations