OnlineFirst Articles
Research Papers

Evaluation of Trichoderma asperellum ICC012 and T. gamsii ICC080 to protect almond pruning wounds from infections caused by fungal trunk pathogens

PDF
  • Hamza Bin SAJID,
  • Maya HACHICHA,
  • Yan-Jiun HUANG,
  • Mónica BERBEGAL,
  • Josep ARMENGOL
Hamza Bin SAJID
Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Spain
Maya HACHICHA
Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Spain
Yan-Jiun HUANG
Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Spain
Mónica BERBEGAL
Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Spain
Josep ARMENGOL
Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Camino de Vera S/N, 46022-Valencia
Bio
DOI: https://doi.org/10.36253/phyto-16809
Categories

Published 2026-03-16

Keywords

  • Diplodia seriata,
  • Eutypa lata,
  • Neofusicoccum parvum,
  • nut crops

How to Cite

[1]
H. B. SAJID, M. HACHICHA, Y.-J. HUANG, M. BERBEGAL, and J. ARMENGOL, “Evaluation of Trichoderma asperellum ICC012 and T. gamsii ICC080 to protect almond pruning wounds from infections caused by fungal trunk pathogens”, Phytopathol. Mediterr., Mar. 2026.

Copyright (c) 2026 Hamza Bin Sajid, Maya Hachicha, Yan-Jiun Huang, Mónica Berbegal, Josep Armengol

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

This study evaluated the potential of Trichoderma asperellum ICC012 and T. gamsii ICC080 to protect almond pruning wounds from infections caused by three major almond trunk pathogens: Diplodia seriata, Eutypa lata, and Neofusicoccum parvum. Dual-culture antagonism assays and two in planta wound protection trials were conducted to assess their efficacy. In the first trial, treatments with T. asperellum ICC012 + T. gamsii ICC080 were applied one or seven days before or after pathogen inoculation to test the impact of application timing, while the second trial focused on preventive strategies, comparing single versus double applications prior to inoculation. Both Trichoderma strains alone and mixed were able to inhibit pathogen growth in vitro. Experiments in planta showed that only pre-infection applications significantly protected pruning wounds, though their efficacy differed by pathogen and treatment strategy. Protection was highest against E. lata and D. seriata, in which a single treatment prevented infection, whereas N. parvum proved more challenging; only a double pre-inoculation application markedly improved its control. Our results demonstrate that preventive wound protection by T. asperellum ICC012 + T. gamsii ICC080 is essential for effective control. Incorporating these biocontrol agents into almond orchard management can substantially reduce trunk disease infections and limit reliance on synthetic fungicides in Mediterranean production systems.

PDF

Downloads

Download data is not yet available.

References

  1. De Mendiburu F., 2023. Agricolae: Statistical Procedures for Agricultural Research, R package version 1.3-7. R Core Team, Vienna, Austria. https://doi.org/10.32614/CRAN.package.agricolae DOI: https://doi.org/10.32614/CRAN.package.agricolae
  2. Di Marco S., Metruccio E.G., Moretti S., Nocentini M., Carella G., …., Mugnai L., 2022. Activity of Trichoderma asperellum strain ICC 012 and Trichoderma gamsii strain ICC 080 toward diseases of Esca complex and associated pathogens. Frontiers in Microbiology 12: 813410. https://doi.org/10.3389/fmicb.2021.813410 DOI: https://doi.org/10.3389/fmicb.2021.813410
  3. Dinno A., 2024. dunn.test: Dunn’s Test of Multiple Comparisons Using Rank Sums, R package version 1.3.6. https://doi.org/10.32614/CRAN.package.dunn.test DOI: https://doi.org/10.1080/00401706.1964.10490181
  4. Elena G., Luque J., 2016. Seasonal susceptibility of grapevine pruning wounds and cane colonization in Catalonia, Spain following artificial infection with Diplodia seriata and Phaeomoniella chlamydospora. Plant Disease 100(8): 1651–1659. https://doi.org/10.1094/PDIS-10-15-1186-RE DOI: https://doi.org/10.1094/PDIS-10-15-1186-RE
  5. FAO, 2024. Food and Agriculture Organization of the United Nations, Statistical Databases. Available at: http://www.fao.org. Accessed March 19, 2024.
  6. Fujiyoshi P.T., Lawrence D.P., Travadon R., Cooper M., Verdegaal P., Schwebs S., Baumgartner K., 2021. Detection of spores of causal fungi of dieback-type trunk diseases in young, asymptomatic vineyards and mature, symptomatic vineyards. Crop Protection 150: 105798. https://doi.org/10.1016/j.cropro.2021.105798 DOI: https://doi.org/10.1016/j.cropro.2021.105798
  7. Goura K., Lahlali R., Bouchane O., Baala M., Radouane N., …Tahiri A., 2023. Identification and characterization of fungal pathogens causing trunk and branch cankers of almond trees in Morocco. Agronomy 13(1): 130. https://doi.org/10.3390/agronomy13010130 DOI: https://doi.org/10.3390/agronomy13010130
  8. Gradziel T.M., 2017. History of cultivation. In: Almonds: Botany, Production and Uses, CABI, Wallingford, United Kingdom, 43–69. https://doi.org/10.1079/9781780643540.0043 DOI: https://doi.org/10.1079/9781780643540.0043
  9. Gramaje D., Agustí-Brisach C., Pérez-Sierra A., Moralejo E., Olmo D., … Armengol J., 2012. Fungal trunk pathogens associated with wood decay of almond trees on Mallorca (Spain). Persoonia: Molecular Phylogeny and Evolution of Fungi 28: 1–13. https://doi.org/10.3767/003158512X626155 DOI: https://doi.org/10.3767/003158512X626155
  10. Guarnaccia V., Kraus C., Markakis E., Alves A., Armengol J., … Gramaje D., 2022. Fungal trunk diseases of fruit trees in Europe: pathogens, spread and future directions. Phytopathologia Mediterranea 61(3): 563–599. https://doi.org/10.36253/phyto-14167 DOI: https://doi.org/10.36253/phyto-14167
  11. Guzmán-Guzmán P., Kumar A., de Los Santos-Villalobos S., Parra-Cota F.I., Orozco-Mosqueda M.D.C., … Santoyo, G., 2023. Trichoderma species: Our best fungal allies in the biocontrol of plant diseases—A review. Plants 12(3), 432. https://doi.org/10.3390/plants12030432 DOI: https://doi.org/10.3390/plants12030432
  12. Holland L.A., Travadon R., Lawrence D.P., Nouri M.T., Trouillas F., 2021a. Evaluation of pruning wound protection products for the management of almond canker diseases in California. Plant Disease 105(11): 3368–3375. https://doi.org/10.1094/PDIS-11-20-2371-RE DOI: https://doi.org/10.1094/PDIS-11-20-2371-RE
  13. Holland L.A., Trouillas F.P., Nouri M.T., Lawrence D.P., Crespo M., … Fichtner E.J., 2021b. Fungal pathogens associated with canker diseases of almond in California. Plant Disease 105(2): 346–360. https://doi.org/10.1094/PDIS-10-19-2128-RE DOI: https://doi.org/10.1094/PDIS-10-19-2128-RE
  14. Inderbitzin P., Bostock R.M., Trouillas F.P., Michailides T.J., 2010. A six locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia 102(6): 1350–1368. https://doi.org/10.3852/10-006 DOI: https://doi.org/10.3852/10-006
  15. Jiménez Luna I., Doll D., Ashworth V.E.T.M., Trouillas F.P., Rolshausen P.E., 2022. Comparative profiling of wood canker pathogens from spore traps and symptomatic plant samples within California almond and walnut orchards. Plant Disease 106(8): 2182–2190. https://doi.org/10.1094/PDIS-05-21-1057-RE DOI: https://doi.org/10.1094/PDIS-05-21-1057-RE
  16. Lahlali R., Ezrari S., Radouane N., Kenfaoui J., Esmaeel Q., … Barka, E. A., 2022. Biological control of plant pathogens: A global perspective. Microorganisms 10(3): 596. https://doi.org/10.3390/microorganisms10030596 DOI: https://doi.org/10.3390/microorganisms10030596
  17. Lawrence D.P., Holland L.A., Nouri M.T., Travadon R., Abramians A., Michailides T.J., Trouillas F.P., 2018. Molecular phylogeny of Cytospora species associated with canker diseases of fruit and nut crops in California, with the descriptions of ten new species and one new combination. IMA Fungus 9(2): 333–369. https://doi.org/10.5598/imafungus.2018.09.02.07 DOI: https://doi.org/10.5598/imafungus.2018.09.02.07
  18. León M., Berbegal M., Rodríguez-Reina J.M., Elena G., Abad-Campos P., …Armengol J., 2020. Identification and characterization of Diaporthe spp. associated with twig cankers and shoot blight of almonds in Spain. Agronomy 10(8): 1062. https://doi.org/10.3390/agronomy10081062 DOI: https://doi.org/10.3390/agronomy10081062
  19. Luque‐Cruz C., Capote N., Marco‐Noales E., Palomares‐Rius J. E., Romero‐Cuadrado L., Morán, F., … Agustí‐Brisach, C., 2026. Insights Into the Aetiology of Almond Canker Diseases and Decline Syndromes: An Emerging and Complex Phytopathological Challenge. Plant Pathology 75: e70126. https://doi.org/10.1111/ppa.70126 DOI: https://doi.org/10.1111/ppa.70126
  20. Markakis E.A., Kavroulakis N., Ntougias S., Koubouris G.C., Sergentani C.K., Ligoxigakis E.K., 2017. Characterization of fungi associated with wood decay of tree species and grapevine in Greece. Plant Disease 101(11): 1929–1940. https://doi.org/10.1094/PDIS-12-16-1761-RE DOI: https://doi.org/10.1094/PDIS-12-16-1761-RE
  21. Martino I., Spadaro D., Guarnaccia V., 2025. Fungal trunk pathogens of fruit and nut tree crops: identification, characterization, detection, and perspectives for a critical global issue. Plant Disease 109(6): 1192–1210. https://doi.org/10.1094/PDIS-10-24-2069-FE DOI: https://doi.org/10.1094/PDIS-10-24-2069-FE
  22. Nouri M.T., Lawrence D.P., Yaghmour M.A., Michailides T.J., Trouillas F.P., 2018. Neoscytalidium dimidiatum causing canker, shoot blight and fruit rot of almond in California. Plant Disease 102(8): 1638–1647. https://doi.org/10.1094/PDIS-12-17-1967-RE DOI: https://doi.org/10.1094/PDIS-12-17-1967-RE
  23. Olmo D., Armengol J., León M., Gramaje D., 2016. Characterization and pathogenicity of Botryosphaeriaceae species isolated from almond trees on the island of Mallorca (Spain). Plant Disease 100(12): 2483–2491. https://doi.org/10.1094/PDIS-05-16-0676-RE DOI: https://doi.org/10.1094/PDIS-05-16-0676-RE
  24. Olmo D., Gramaje D., Armengol J., 2017. Evaluation of fungicides to protect pruning wounds from Botryosphaeriaceae species infections on almond trees. Phytopathologia Mediterranea 56: 118–129. https://doi.org/10.14601/Phytopathol_Mediterr-19428
  25. R Core Team, 2024. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  26. Rinu K., Sati P., Pandey A., 2014. Trichoderma gamsii (NFCCI 2177): a newly isolated endophytic, psychrotolerant, plant growth promoting, and antagonistic fungal strain. Journal of Basic Microbiology 54(5): 408–417. https://doi.org/10.1002/jobm.201200579 DOI: https://doi.org/10.1002/jobm.201200579
  27. Romero-Cuadrado L., Picos M.C., Camacho M., Ollero F.J., Capote N., 2024. Biocontrol of almond canker diseases caused by Botryosphaeriaceae fungi. Pest Management Science 80(4): 1839–1848. https://doi.org/10.1002/ps.7919 DOI: https://doi.org/10.1002/ps.7919
  28. Rueden C.T., Schindelin J., Hiner M.C., DeZonia B.E., Walter A.E., Arena E.T., Eliceiri K.W., 2017. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18(1): 529. https://doi.org/10.1186/s12859-017-1934-z DOI: https://doi.org/10.1186/s12859-017-1934-z
  29. Slippers B., Smit W.A., Crous P.W., Coutinho T.A., Wingfield B.D., Wingfield M.J., 2007. Taxonomy, phylogeny and identification of Botryosphaeriaceae associated with pome and stone fruit trees in South Africa and other regions of the world. Plant Pathology 56(1): 128–139. https://doi.org/10.1111/j.1365-3059.2006.01486.x DOI: https://doi.org/10.1111/j.1365-3059.2006.01486.x
  30. Travadon R., Lawrence D.P., Li S., Trouillas F.P., 2023a. Evaluation of biological control agents for the protection of almond pruning wounds against infection by fungal canker pathogens. Phytopathology 113(8): 1417–1427. https://doi.org/10.1094/PHYTO-02-23-0075-R DOI: https://doi.org/10.1094/PHYTO-02-23-0075-R
  31. Travadon R., Lawrence D.P., Li S., Trouillas F.P., 2023b. Field evaluation of biological wound treatments for the management of almond, cherry, and grapevine fungal canker diseases. Biological Control 185: 105292. https://doi.org/10.1016/j.biocontrol.2023.105292 DOI: https://doi.org/10.1016/j.biocontrol.2023.105292
  32. Travadon R., Rolshausen P.E., Gubler W.D., Cadle-Davidson L., Baumgartner K., 2013. Susceptibility of cultivated and wild Vitis spp. to wood infection by fungal trunk pathogens. Plant Disease 97(12): 1529–1536. https://doi.org/10.1094/PDIS-05-13-0525-RE DOI: https://doi.org/10.1094/PDIS-05-13-0525-RE
  33. Úrbez-Torres J.R., Battany M., Bettiga L.J., Gispert C., McGourty G., Roncoroni J., Smith R.J., Verdegaal P., Gubler W.D., 2010. Botryosphaeriaceae species spore-trapping studies in California vineyards. Plant Disease 94(6): 717–724. https://doi.org/10.1094/PDIS-94-6-0717 DOI: https://doi.org/10.1094/PDIS-94-6-0717
  34. Úrbez-Torres J.R., Tomaselli E., Pollard-Flamand J., Boule J., Gerin D., Pollastro S., 2020. Characterization of Trichoderma isolates from southern Italy, and their potential biocontrol activity against grapevine trunk disease fungi. Phytopathologia Mediterranea 59(3): 425–440. https://doi.org/10.14601/Phyto-11273
  35. Verma M., Brar S.K., Tyagi R.D., Surampalli R.Y., Valéro J.R., 2007. Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochemical Engineering Journal 37(1): 1–20. https://doi.org/10.1016/j.bej.2007.05.012 DOI: https://doi.org/10.1016/j.bej.2007.05.012
  36. Wu Q., Sun R., Ni M., Yu J., Li Y., Yu C., Dou K., Ren J., Chen J., 2017. Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLOS ONE 12: 1–20. https://doi.org/10.1371/journal.pone.0179957 DOI: https://doi.org/10.1371/journal.pone.0179957

Most read articles by the same author(s)

1 2 > >>