Investigation of the Effectiveness of Clonostachys rosea (Sch.) Schroers & Samuels on Root Rot Caused by Fusarium solani (March.) Sacc. in Pistachio (Pistacia vera L.)

Öz

This study was conducted in the Phytopathology Laboratory and controlled-environment growth chamber of Siirt University during 2022-2023 to evaluate the efficacy of Clonostachys rosea against root rot caused by Fusarium solani in pistachio (Pistacia vera L.). The study material included F. solani KY1, previously isolated from pistachio roots and identified as pathogenic, along with C. rosea isolates F8, F9, and F10, also obtained from the pistachio root region, and the LO41 isolate obtained from the Phytopathology Laboratory collection. According to the results of the experiment evaluating the antagonistic activity of volatile metabolites produced by C. rosea isolates, F10 was the most effective, inhibiting the pathogen by 9.04%. In the dual culture assay, the LO41 isolate exhibited the strongest antagonistic effect against the pathogen, with 17.20% inhibition. However, regarding the antagonists’ ability to overgrow and parasitize the hyphae of the pathogen, all isolates, except C. rosea F9, exhibited markedly stronger hyperparasitic activity. In the pot experiment conducted to evaluate the efficacy of the antagonists in soil artificially contaminated with F. solani, the disease severity in the positive control (F. solani KY1) was 72.50%. Following the application of C. rosea isolates F10, F8, LO41, and F9, disease severity was reduced to 20.00%, 27.50%, 37.50%, and 52.50%, respectively. The pathogen suppression rates of the antagonists were 72.41%, 62.06%, 48.27%, and 27.58%, respectively, indicating that C. rosea F10 was the most effective isolate. Consequently, the capability of C. rosea as a biological control agent against F. solani, a major soil-borne pathogen in pistachios, was further investigated.

Anahtar Kelimeler

• Pistachios
• root rot
• Clonostachys rosea
• Fusarium solani
• biological control

Kaynakça

1. Anonymous, 2025. Production Statistics. Food and Agriculture Organization of the United Nations, (http://www.fao.org/faostat/en/#data), (Accessed: 12.03.2025).
2. Arie, T., 2019. Fusarium diseases of cultivated plants, control, diagnosis, and molecular and genetic studies. Journal of Pesticide Science, 44(4): 275-281.
3. Aydın, M.H., 2019. Determination of diseases of pistachio (Pistacia vera L.) in Siirt, Turkey. I. International Harran Multidisciplinary Studies Congress, 8-10 March, Şanlıurfa, Turkey, pp. 61-64. (In Turkish).
4. Aydın, M.H., Canpolat, S., Uzun, T., 2024. Some soilborne pathogens causing root rot and wilting of pistachio trees in southeastern Turkey. Canadian Journal of Plant Pathology, 46(4): 395-409.
5. Aydın, M.H., İnal, B., Uzun, T., Aydın, Y., Kayalar, B., 2023. Investigation of fungal causal agents root rot and wilt on pistachio (Pistacia vera L.) orchard: Siirt province location, Türkiye. Turkish Journal of Agricultural Research, 10(3): 308-319. (In Turkish).
6. Aydın, M.H., Turhan, G., 2009. Studies on determination of fungal antagonists of Rhizoctonia solani. Anadolu Journal of Aegean Agricultural Research Institute, 19(2): 49-72.
7. Aydın, M.H., Ünal, F., 2021. Anastomosis groups and pathogenicity of Rhizoctonia solani Kühn ısolates obtained from pistachio (Pistacia vera L.) saplings in Siirt province, Turkey. Turkish Journal of Agricultural Research, 8(1): 18-26.
8. Barnett, H.L., Lilly, V.G., 1962. A destructive mycoparasite, Gliocladium roseum. Mycologia, 54(1): 72-77.

9. Beccari, G., Hao, G., Liu, H., 2022. Editorial: Fusarium pathogenesis: Infection mechanisms and disease progression in host plants. Frontiers of Plant Science, 13: 1020404.
10. Chatterton, S., Punja, Z.K., 2009. Chitinase and beta-1,3-glucanase enzyme production by the mycoparasite Clonostachys rosea F. catenulata against fungal plant pathogens. Canadian Journal of Microbiology, 55(4): 356-367.
11. Chitzanidis, A., 1995. Pistachio diseases in greece. Acta Horticulturae, 419(57): 345-348.
12. Crespo Palomo, M., Lawrence, D., Nouri, M., Doll, D., Trouillas, F., 2019. Characterization of Fusarium and Neocosmospora species associated with crown rot and stem canker of pistachio rootstocks in California. Plant Disease, 103(8): 1931-1939.
13. Çevik, R., Demir, S., Türkölmez, Ş., Boyno, G., 2022. The effect of Clonostachys rosea (Sch.) schroers and samuels against verticillium wilt (Verticillium dahliae Kleb.) and early blight [Alternaria solani (Ell. and G. Martin) Sor.] diseases in tomato plants. Yuzuncu Yıl University Journal of Agricultural Sciences, 32(2): 372-382.
14. Dennis, C., Webster, J., 1971. Antagonistic properties of species groups of Trichoderma II. Production of volatile antibiotics. Transactions of the British Mycological Society, 57(1): 41-48.
15. Eskalen, A., Küsek, M., Danıştı, L., Karadağ, S., 2001. Fungal diseases in pistachio trees in East-Mediterranean and Southeast Anatolian Regions. Cahiers Options Mediterraneennes, 56(1): 261-264.
16. Fatema, U., Broberg, A., Jensen, D.F., Karlsson, M., Dubey, M., 2018. Functional analysis of polyketide synthase genes in the biocontrol fungus Clonostachys rosea. Scientific Reports, 8(1): 15009.
17. García, R.A.M., Martijn ten Hoopen, G., Kass, D.C.J., Sánchez Garita, V.A., Krauss, U., 2003. Evaluation of mycoparasites as biocontrol agents of Rosellinia root rot in cocoa. Biological Control, 27(2): 210-227.
18. Haarith, D., Bushley, K.E., Chen, S., 2020. Fungal communities associated with Heterodera glycines and their potential in biological control: A current update. Journal of Nematology, 52(1): 1-17.
19. Jensen, B., Knudsen, I.M.B., Madsen, M., Jensen, D.F., 2004. Biopriming of infected carrot seed with an antagonist, Clonostachys rosea, selected for control of seedborne Alternaria spp. Phytopathology, 94(6): 551-560.
20. Jensen, B., Lübeck, P.S., Jorgensen, H.J.L., 2016. Clonostachys rosea reduces spot blotch in barley by inhibiting pre-penetration growth and sporulation of Bipolaris sorokiniana without inducing resistance. Pest Management Science, 72(12): 2231-2239.
21. Jensen, D.F., Dubey, M., 2022. Clonostachys rosea to control plant diseases. In: J. Köhl and W. Ravensberg (Eds.), Microbial Bioprotectants for Plant Disease Management, Burleigh Dodds Science Publishing, Cambridge, UK, pp. 429-472.
22. Kosawang, C., Karlsson, M., Jensen, D.F., Dilokpimol, A., Collinge, D.B., 2014. Transcriptomic profiling to identify genes involved in Fusarium mycotoxin deoxynivalenol and zearalenone tolerance in the mycoparasitic fungus Clonostachys rosea. BMC Genomic, 15(55): 1-11.
23. Krauss, U., Soberanis, W., 2001. Biocontrol of cocoa pod diseases with mycoparasite mixtures. Biological Control, 22(2): 149-158.
24. Kulik, T., Treder, K., Rochoń, M., Załuski, D., Sulima, P., Olszewski, J., Bilska, K., Elena, G., Kowalski, T., 2024. Measurement of the effectiveness of Clonostachys rosea in reducing Fusarium biomass on wheat straw. Journal of Applied Genetics, 65(1): 937-947.
25. Leslie, J.F., Summerell, B., 2013. An overview of Fusarium. In: D.W. Brown and R.H. Proctor (Eds.), Fusarium Genomics, Molecular and Cell Biology, Caister Academic Press, pp. 1-9.
26. Lysøe, E., Dees, M.W., Brurberg, M.B., 2017. A three-way transcriptomic interaction study of a biocontrol agent (Clonostachys rosea), a fungal pathogen (Helminthosporium solani), and a potato host (Solanum tuberosum). Molecular Plant-Microbe Interactions, 30(8): 646-655.
27. Michailides, T.J., Morgan, D.P., Doster, M.A., 1995. Diseases of pistachio in california and their significance. Acta Horticulturae, 419(1): 337-343.
28. Mouekouba, L.D., Zhang, L., Guan, X., Chen, X., Chen, H., Zhang, J., Zhang, J., Li, J., 2014. Analysis of Clonostachys rosea-induced resistance to tomato gray mold disease in tomato leaves. Plos One, 9(7): 155-175.
29. Nganje, W.E., Bangsund, D.A., Leistritz, F.L., Wilson, W.W., Tiapo, N.M., 2004. Regional economic impacts of Fusarium head blight in wheat and barley. Applied Economic Perspectives and Policy, 26(1): 332-347.
30. Nobre, S.A.M., Maffia, L.A., Mizubuti, E.S.G., Cota, L.V., Dias, A.P.S., 2005. Selection of Clonostachys rosea isolates from Brazilian ecosystems effective in controlling Botrytis cinerea. Biological Control, 34(2): 132-143.
31. Nouri, M., Holland, L., Doll, D., Kallsen, C., Michailides, T., Trouillas, F., 2018. Investigating canker and soil borne diseases of pistachio in California. Acta Horticulturae, 1219(1): 295-302.
32. Nygren, K., Dubey, M., Zapparata, A., Iqbal, M., Tzelepis, G.D., Durling, M.B., Jensen, D.F., Karlsson, M., 2018. The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey. Evolutionary Applications, 11(6): 931-949.
33. Roberti, R., Veronesi, A., Cesari, A., Cascone, A., Di Berardino, I., Bertini, L., Caruso, C., 2008. Induction of PR proteins and resistance by the biocontrol agent Clonostachys rosea in wheat plants infected with Fusarium culmorum. Plant Science, 175(3): 339-347.
34. Salas-Salvadó, J., Casas-Agustench, P., Salas-Huetos, A., 2011. Cultural and historical aspects of mediterranean nuts with emphasis on their attributed healthy and nutritional properties. Nutrition, Metabolism and Cardiovascular Diseases, 21(1): S1-S6.
35. Samsudin, N.I.P., Rodriguez, A., Medina, A., Magan, N., 2017. Efficacy of fungal and bacterial antagonists for controlling growth, FUM1 gene expression and fumonisin B1 production by Fusarium verticillioides on maize cobs of different ripening stages. International Journal of Food Microbiology, 246(1): 72-79.
36. Schöneberg, A., Musa, T., Voegele, R.T., Vogelgsang, S., 2015. The potential of antagonistic fungi for control of Fusarium graminearum and Fusarium crookwellense varies depending on the experimental approach. Journal of Applied Microbiology, 118(5): 1165-1179.
37. Schroers, H.J., Samuels, G.J., Seifert, K.A., Gams, W., 1999. Classification of the mycoparasite Gliocladium roseum in Clonostachys as C. rosea, its relationship to Bionectria ochroleuca and notes on other Gliocladium-like fungi. Mycologia, 91(1): 365-385.
38. Shravani, V., Govindasamy, J., Annaiyan, S., Iruthayasamy, J., Nallusamy, S., Eswaran, K., Venkatesan, P., 2025. One fungus, two foes: Clonostachys rosea as a biocontrol agent against root-knot nematode (Meloidogyne incognita) and Fusarium wilt disease complex in ridge gourd. Archives of Microbiology, 207(9): 209-217.
39. Sun, Z.B., Li, S.D., Ren, Q., Xu, J.L., Lu, X., Sun, M.H., 2020. Biology and applications of Clonostachys rosea. Journal of Applied Microbiology, 129(3): 486-495.
40. Sun, Z.B., Sun, M.H., Li, S.D., 2015. Identification of mycoparasitism-related genes in Clonostachys rosea 67-1 active against Sclerotinia sclerotiorum. Scientific Report, 5: 18169.
41. Sutton, J.C., Li, D.W., Peng, G., Yu, H., Zhang, P., Valdebenito-Sanhueza, R.M., 1997. Gliocladium roseum- A versatile adversary of Botrytis cinerea in crops. Plant Disease, 81(4): 316-328.
42. Triki, M.A., Rhouma, A., Chaabouni, A.C., Ioos, R., 2011. Emergence of Fusarium solani causing root rot of pistachio trees in Tunisia. Acta Horticulturae, 912(1): 717-721.
43. Turhan, G., 1990. Further hyperparasites of Rhizoctonia solani Kühn as promising candidates for biological control. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz, 97(1): 208-215.
44. Turhan, G., 1992. Unterdrückrung des Rhizoctonia-Befalls durch einen neuen Mykoparasiten, Stachybotrys Elegans, 48. Deutsche Pflanzen Schuztagung, Göttingen (FRG).
45. Türkölmez, Ş., Çiftçi, O., Derviş, S., Ulubaş, Ç., 2015. First report of Phytophthora palmivora causing crown and root rot of pistachio trees in Turkey. Plant Disease, 99(12): 1866.
46. Verdejo-Lucas, S., Ornat, C., Sorribas, F.J., Stchiegel, A., 2002. Species of root-knot nematodes and fungal egg parasites recovered from vegetables in Almeria and Barcelona, Spain. Journal of Nematology, 34(4): 405-408.
47. Vincent, J.M., 1947. Distortion of fungal hyphae in the presence of certain inhibitors. Nature, 159: 850.
48. Wang, Q.Y., Chen, X.L., Chai, X.F., Xue, D., Zheng, W., Shi, Y., Wang, A., 2019. The involvement of jasmonic acid, ethylene, and salicylic acid in the signaling pathway of Clonostachys rosea-induced resistance to gray mold disease in tomato. Phytopathology, 109(7): 1102-1114.
49. Yohalem, D.S., Nielsen, K., Green, H., Funck, J.D., 2004. Biocontrol agents efficiently inhibit sporulation of Botrytis aclada on necrotic leaf tips but spread to adjacent living tissue is not prevented. Federation of European Microbiological Societies, Microbiology Ecology, 47(3): 297-303.