Research Article
BibTex RIS Cite

Domateste Botrytis cinerea'nın kontrolünde antagonistler: Olası inhibitörlerin moleküler bağlanma üzerine in vitro değerlendirme ve in silico tarama

Year 2025, Volume: 12 Issue: 3, 870 - 886, 23.07.2025
https://doi.org/10.30910/turkjans.1619273

Abstract

Bu çalışma, Botrytis cinerea patojenine karşı Clonostachys rosea, Trichoderma harzianum ve Bacillus mojavensis aday antagonistlerinin antifungal etkilerini ve aday antagonistlerinin karşılıklı etkileşimlerini, moleküler bağlanma analiziyle de in vitro ve in silico etkileşimlerini incelemek amacıyla yürütülmüştür. Çalışmada aday antagonist uygulamalarının B. cinerea M2-1 izolatının misel gelişimi üzerine etkilerine bakıldığında % 56 oranı ile en etkili izolatın T. harzianum C7-3 olduğu, bu izolatı %32 oranı ile B. mojavensis K193 ve %26 oranı ile C. rosea C6-4 izolatlarının takip ettiği belirlenmiştir. Aday antagonist izolatlarının karşılıklı etkileşimleri değerlendirildiğinde T. harzianum’un C. rosea’nın misel gelişimini kontrole oranla azalttığı belirlenmiştir. T. harzianum × B. mojavensis eşleştirilmesinde fungal antagonistin misel gelişimi bakteriyel izolat ile karşılaştıkları hatta bakteriyel izolat tarafından engellenmiştir. C. rosea × B. mojavensis eşleştirmesinde C. rosea’nın yavaş gelişimi değerlendirilen süre sonunda bakteriyel izolat ile karşılaşmamasına neden olmuştur. Çalışmada ayrıca patojen ve aday antagonistlerin domates tohumlarının (cv. Süper) kök ve sürgün uzunluğu ölçülmüş ve çimlenme yüzdeleri hesaplanmıştır. C. rosea (3,09 cm) ve B. mojavensis (3,57 cm) izolatları tohumların sürgün gelişimlerini, B. mojavensis K193 izolatı (4,02 cm) tohumların kök gelişimini, T. harzianum C7-3 izolatı ise tohumların çimlenme yüzdesini (%86,7) kontrole oranla artırmıştır. Moleküler bağlanma bulguları, T. harzianum'dan elde edilen ligandların kombinasyonunun, patojenite ve virülanslıkla ilişkili proteinleri inhibe veya modifiye ederek B. cinerea'ya karşı antifungal etkinliği sinerjik bir şekilde artırabileceğini göstermiştir. In silico çalışma sonuçları, T. harzianum kaynaklı metabolitlerin B. cinerea proteinleri üzerindeki etkilerini ve etkileşimlerini doğrulamak için daha fazla laboratuvar araştırmasına ihtiyaç olduğunu göstermiştir.

References

  • Akbaba, M., Özaktan, H. (2018). Biocontrol of angular leaf spot disease and colonization of cucumber (Cucumis sativus L.) by endophytic bacteria. Egyptian Journal of Biological Pest Control, 28: 1-10.
  • Alina, SO., Constantinscu, F., Petruţa, CC. (2015). Biodiversity of Bacillus subtilis group and beneficial traits of Bacillus species useful in plant protection. Romanian Biotechnological Letters, 20(5), 10737–10750.
  • Amarouchi, Z., Esmaeel, Q., Sanchez, L., Jacquard, C., Hafidi, M., Vaillant-Gaveau, N., Ait Barka, E. (2021). Beneficial microorganisms to control the gray mold of grapevine: From screening to mechanisms. Microorganisms, 9(7): 1386.
  • Anderson, AC., Stangherlin, S., Pimentel, KN., Weadge, JT., Clarke, AJ. (2022). The SGNH hydrolase family: A template for carbohydrate diversity. Glycobiology, 32(10), 826–848.
  • Blake, C., Christensen, MN., Kovács, ÁT. (2021). Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Molecular Plant-Microbe Interactions, 34(1): 15–25.
  • Boddy, L. (2016). Pathogens of autotrophs. In The fungi (pp. 245–292). Academic Press.
  • Bolivar-Anillo, HJ., González-Rodríguez, VE., Cantoral, JM., García-Sánchez, D., Collado, IG., Garrido, C. (2021). Endophytic bacteria Bacillus subtilis, isolated from Zea mays, as potential biocontrol agent against Botrytis cinerea. Biology, 10(6): 492.
  • Calvo, P., Ormeño-Orrillo, E., Martínez-Romero, E., Zúñiga, D. (2010). Characterization of Bacillus isolates of potato rhizosphere from Andean soils of Peru and their potential PGPR characteristics. Brazilian Journal of Microbiology, 41(4): 899–906.
  • Carillo, P., Woo, SL, Comite, E., El-Nakhel, C., Rouphael, Y., Fusco, GM., Borzacchiello, A., Lanzuise, S., Vinale, F. (2020). Application of Trichoderma harzianum, 6-pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants, 9(6): 771.
  • Cheng, L., Liu, J., Liu, J., Guo, D., Deng, F., Bian Q, et al. (2023). Design, synthesis, antifungal activity and molecular docking of ring-opened pimprinine derivative containing (thio) amide structure. Pest Management Science, 79 (7): 2220–2229.
  • Christopher, DJ., Raj, TS., Rani, SU., Udhayakumar, R. (2010). Role of defense enzymes activity in tomato as induced by Trichoderma virens against Fusarium wilt caused by Fusarium oxysporum f. sp. lycopersici. Journal of Biopesticides, 3(1), 158.
  • Cota, LV., Maffia, LA., Mizubuti, ESG. (2008). Brazilian isolates of Clonostachys rosea: Colonization under different temperature and moisture conditions and temporal dynamics on strawberry leaves. Letters in Applied Microbiology, 46(3): 312–317.
  • Cui, Z., Gao, N., Wang, Q., Ren, Y., Wang, K., Zhu, T. (2015). BcMctA, a putative monocarboxylate transporter, is required for pathogenicity in Botrytis cinerea. Current Genetics, 61(4): 545–553.
  • de Nadal, E., Posas, F. (2009). Multilayered control of gene expression by stress-activated protein kinases. EMBO Journal, 29(4): 4–13.
  • Dean, R., Van Kan, JA., Pretorius, ZA., Hammond‐Kosack, KE., Di Pietro, A., Spanu, PD., Foster, GD. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13(4): 414–430.
  • Demirel, F. (2021). In silico analysis of protein disulfide isomerases in soybean. Journal of Agriculture, 4(1): 48–56.
  • Demirel, S., Güller, A., Usta, M., Kurt, Z., Korkmaz, G. (2024). Coat protein of alfalfa mosaic alfamovirus (AMV) from Türkiye: Genetic inference and in silico docking analysis for potential antiphytoviral purposes. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(1): 13529.
  • Diabankana, RGC., Afordoanyi, DM., Safin, RI., Nizamov, RM., Karimova, LZ., Validov, SZ. (2021). Antifungal properties, abiotic stress resistance, and biocontrol ability of Bacillus mojavensis PS17. Current Microbiology, 78(8): 3124–3132.
  • Earl, AM., Eppinger, M., Fricke, WF., Rosovitz, MJ., Rasko, DA., Daugherty, S., Losick, R., Kolter, R., Ravel, J. (2012). Whole-genome sequences of Bacillus subtilis and close relatives. Journal of Bacteriology, 194(9): 2378–2379.
  • Eken, C., Genç T., S. Tuncer ve Z. Kadıoğlu. (2013). Çilekte kurşuni küf hastalığı etmeni Botrytis cinerea’ya in vitroda fungal antagonistlerin etkisi. Türkiye 5. Organik Tarım Sempozyumu, 25-27 Eylül, Samsun, Türkiye.
  • Elad, Y., Pertot, I., Prado, AMC., Stewart, A. (2016). Plant hosts of Botrytis spp. In Botrytis: The fungus, the pathogen and its management in agricultural systems (pp. 413–486). Springer.
  • Enebe, MC., Babalola, OO. (2019). The impact of microbes in the orchestration of plants’ resistance to biotic stress: A disease management approach. Applied Microbiology and Biotechnology, 103(1): 9–25.
  • Fan, J., Fu, A., Zhang, L. (2019). Progress in molecular docking. Quantitative Biology, 7(1): 83–89.
  • Fiorini, L., Guglielminetti, L., Mariotti, L., Curadi, M., Picciarelli, P., Scartazza, A., Vannacci, G. (2016). Trichoderma harzianum T6776 modulates a complex metabolic network to stimulate tomato cv. Micro-Tom growth. Plant and Soil, 400: 351-366.
  • Fira, D., Dimkić, I., Berić, T., Lozo, J., Stanković, S. (2018). Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285(1): 44–55.
  • Gelmez, C., Müftüoğlu, NM. (2018). Effect of different calcium doses and nitrogen fertilizers on yield and yield characteristic in tomatoes. Journal of Graduate School of Natural and Applied Sciences, 4(2): 134–148.
  • Geng, L., Fu, Y., Peng, X., Yang, Z., Zhang, M., Song, Z. (2022). Biocontrol potential of Trichoderma harzianum against Botrytis cinerea in tomato plants. Biological Control, 174(1): 105019.
  • Grabka, R., d’Entremont, TW., Adams, SJ., Walker, AK., Tanney, JB., Abbasi, PA., Ali, S. (2022). Fungal endophytes and their role in agricultural plant protection against pests and pathogens. Plants, 11(3): 384.
  • Guzmán-Guzmán, P., Kumar, A., de Los Santos-Villalobos, S., Parra-Cota, FI., Orozco-Mosqueda, MDC., Fadiji, AE. (2023). Trichoderma species: Our best fungal allies in the biocontrol of plant diseases—A review. Plants, 12(3): 432.
  • Hahn, M. (2014). The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. Journal of Chemical Biology, 7(4): 133–141.
  • Hammad, M., Guillemette, T., Alem, M., Bastide, F., Louanchi, M. (2021). First report of three species of Trichoderma isolated from the rhizosphere in Algeria and the high antagonistic effect of Trichoderma brevicompactum to control grey mould disease of tomato. Egyptian Journal of Biological Pest Control, 31(1): 85.
  • Han, Z., Ghanizadeh, H., Zhang, H., Li, X., Li, T., Wang, Q., Liu, J., Wang, A. (2022). Clonostachys rosea promotes root growth in tomato by secreting auxin produced through the tryptamine pathway. Journal of Fungi, 8(11): 1166.
  • Hang, NTT., Oh, SO., Kim, GH., Hur, JS., Koh, YJ. (2005). Bacillus subtilis S1-0210 as a biocontrol agent against Botrytis cinerea in strawberries. The Plant Pathology Journal, 21 (1): 59-63.
  • Kesimci, TG., Dönmez, MF. (2022). Determining of the antagonist effects of bacteria againts Botrytis cinerea in strawberry under in vitro conditions. Yuzuncu Yil University Journal of the Institute of Natural and Applied Sciences, 27 (3): 535-547.
  • Khalil, AMA., Abdelaziz, AM., Khaleil, MM., Hashem, AH. (2021). Fungal endophytes from leaves of Avicennia marina growing in semi-arid environment as a promising source for bioactive compounds. Letters in Applied Microbiology, 72: 263–274.
  • Kiesewalter, HT., Lozano-Andrade, CN., Maróti, G., Snyder, D., Cooper, VS., Jørgensen, TS., Kovács, ÁT. (2020). Complete genome sequences of 13 Bacillus subtilis soil isolates for studying secondary metabolite diversity. Microbiology Resource Announcements, 9(2): 10-1128.
  • Krauss, U., Ten Hoopen, M., Rees, R., Stirrup, T., Argyle, T., George, A, ... Casanoves, F. (2013). Mycoparasitism by Clonostachys byssicola and Clonostachys rosea on Trichoderma spp. from cocoa (Theobroma cacao) and implication for the design of mixed biocontrol agents. Biological Control, 67(3): 317-327.
  • Kredics, L., Antal, Z., Manczinger, L., Szekeres, A., Kevei, F., Nagy, E. (2003). Influence of environmental parameters on Trichoderma strains with biocontrol potential. Food Technology and Biotechnology, 41(1): 37-42.
  • Kumar, M. Ashraf S. (2017). Role of Trichoderma spp. as a biocontrol agent of fungal plant pathogens. Probiotics and Plant Health, 497-506.
  • Kumar, SM., Chowdappa, P., Krishna, V. (2015). Development of seed coating formulation using consortium of Bacillus subtilis OTPB1 and Trichoderma harzianum OTPB3 for plant growth promotion and induction of systemic resistance in field and horticultural crops. Indian Phytopathology, 68(1): 25-31.
  • Lahlali, R., Ezrari, S., Radouane, N., Kenfaoui, J., Esmaeel, Q., El Hamss H., ... Barka, EA. (2022). Biological control of plant pathogens: A global perspective. Microorganisms, 10(3): 596.
  • Li, F., Ghanizadeh, H., Song, W., Miao, S., Wang, H., Chen, X., ... Wang, A. (2023). Combined use of Trichoderma harzianum and Clonostachys rosea to manage Botrytis cinerea infection in tomato plants. European Journal of Plant Pathology, 167(4): 637-650.
  • Mamiev, MS., Khakimov, AA., Zuparov, MA., Rakhmonov, UN. (2020). Effectiveness of different fungicides in controlling Botrytis grey mould of tomato. In IOP Conference Series: Earth and Environmental Science 614 (1), December, p. 012112, IOP Publishing.
  • Martínez-Absalón, S., Rojas-Solís, D., Hernández-León, R., Prieto-Barajas, C., Orozco-Mosqueda, MDC., Peña-Cabriales, JJ., .. Santoyo, G. (2014). Potential use and mode of action of the new strain Bacillus thuringiensis UM96 for the biological control of the grey mould phytopathogen Botrytis cinerea. Biocontrol Science and Technology, 24(12), 1349-1362.
  • Meng, F., Lv, R., Cheng, M., Mo, F., Zhang, N., Qi H, ... Wang, A. (2022). Insights into the molecular basis of biocontrol of Botrytis cinerea by Clonostachys rosea in tomato. Scientia Horticulturae, 291: 110547.
  • Mónaco, C., Dal Bello, G., Rollán, MC., Ronco, L., Lampugnani, G., Arteta, N., ... Stocco, M. (2009). Biological control of Botrytis cinerea on tomato using naturally occurring fungal antagonists. Archives of Phytopathology and Plant Protection, 42(8): 729-737.
  • Moriwaki, A., Kubo, E., Arase, S., Kihara, J. (2006). Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol Lett. 257:253-261.
  • Mouekouba, LDO., Zhang, L., Guan, X., Chen, X., Chen, H., Zhang, J., ... Wang, A. (2014). Analysis of Clonostachys rosea-induced resistance to tomato gray mold disease in tomato leaves. PLoS One, 9(7): e102690.
  • Muniroh, MS., Nusaibah, SA., Vadamalai, G., Siddique, Y. (2019). Proficiency of biocontrol agents as plant growth promoters and hydrolytic enzyme producers in Ganoderma boninense infected oil palm seedlings. Current Plant Biology, 20, 100116.
  • Nawrocka, J., Szymczak, K., Maćkowiak, A., Skwarek-Fadecka, M., Małolepsza, U. (2022). Determination of reactive oxygen or nitrogen species and novel volatile organic compounds in the defense responses of tomato plants against Botrytis cinerea induced by Trichoderma virens TRS 106. Cells, 11(19), 3051.
  • Özden, E. (2019). The Effect of pre-sown treatments on seed viability and physiology in tomato. In: AGROFOOD-International Conference on Agronomy and Food Science and Technology, 20-21 Haziran, İstanbul, Türkiye, 394-401.
  • Pandit, MA., Kumar, J., Gulati, S., Bhandari, N., Mehta, P., Katyal, R., Kaur, J. (2022). Major biological control strategies for plant pathogens. Pathogens, 11(2): 273.
  • Pettersen, EF., Goddard, TD., Huang, CC., Couch, GS., Greenblatt, DM., Meng, EC., et al. (2004). UCSF Chimera—avisualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13):1605–12. Plaza, V., Lagües, Y., Carvajal, M., Pérez-García, LA., Mora-Montes, HM., Canessa, P., Larrondo, LF., Castillo, L. (2015). bcpmr1 encodes a P-type Ca2+/Mn2+-ATPase mediating cell-wall integrity and virulence in the phytopathogen Botrytis cinerea. Fungal Genetics and Biology, 76: 36–46
  • Poveda, J., Barquero, M., González-Andrés, F. (2020). Insight into the microbiological control strategies against Botrytis cinerea using systemic plant resistance activation. Agronomy, 10(11): 1822.
  • Rahila, R., Harish, S., Kalpana, K., Anand, G., Arulsamy, M., Kalaivanan, R. (2023). Antifungal metabolites of Streptomyces chrestomyceticus STR-2 inhibits Magnaporthe oryzae, the incitant of rice blast. Current Microbiology, 80(4): 107.
  • Risoli, S., Cotrozzi, L., Sarrocco, S., Nuzzaci, M., Pellegrini, E., Vitti, A. (2022). Trichoderma-induced resistance to Botrytis cinerea in Solanum species: A meta-analysis. Plants, 11(2): 180.
  • Roca-Couso, R., Flores-Félix, JD., Rivas, R. (2021). Mechanisms of action of microbial biocontrol agents against Botrytis cinerea. Journal of Fungi (Basel, Switzerland), 7(12): 1045. https://doi.org/10.3390/jof7121045
  • Saddek, D., Messgo-Moumene, S., Chemat-Djenni, Z., Bendifallah, L., Bencheikh, K. (2020). Antagonism of isolates of Trichoderma spp. against Botrytis cinerea Pers., the agent of gray rot of tomato (Lycopersicum esculentum Mill.) under greenhouse conditions. Journal of Fundamental and Applied Sciences, 12(2): 583–606.
  • Sancaktaroğlu, S., Yıldırım, B., Ekici, K., Demirel, F. (2023). Characterization of essential oil and in silico modeling perspectives of thyme (Thymus eigii M. Zohary et P.H. Davis) jalas species. Iğdır Üniversitesi Tarım Bilimleri Dergisi, 1(2): 52–60.
  • Saraiva, RM., Czymmek, KJ., Borges, AV., Caires, NP., Maffia, LA. (2015). Confocal microscopy study to understand Clonostachys rosea and Botrytis cinerea interactions in tomato plants. Biocontrol Science and Technology, 25(1): 56–71.
  • Saravanakumar, K., Yu, C., Dou, K., Wang, M., Li, Y., Chen, J. (2016). Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall-degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. cucumerinum. Biological Control, 94: 37–46.
  • Saravanakumar, K., Lu, Z., Xia, H., Wang, M., Sun, J., Wang, S., .Chen, J. (2018). Triggering the biocontrol of Botrytis cinerea by Trichoderma harzianum through inhibition of pathogenicity and virulence-related proteins. Biological Control, 123: 53–62.
  • Sati, D., Joshi, T., Pandey, SC., Pande, V., Mathpal, S., Chandra, S., Samant, M. (2022). Identification of putative elicitors from plant root exudates responsible for PsoR activation in plant-beneficial Pseudomonas spp. by docking and molecular dynamics simulation approaches to decipher plant–microbe interaction. Frontiers in Plant Science, 13, 875494.
  • Schaeffer, HJ., Weber, MJ. (1999). Mitogen-activated protein kinases: Specific messages from ubiquitous messengers. Molecular and Cellular Biology, 19(4), 2435–2444.
  • Senkovs, M., Nikolajeva, V., Makarenkova, G., Petrina, Z. (2021). Influence of Trichoderma asperellum and Bacillus subtilis as biocontrol and plant growth-promoting agents on soil microbiota. Annals of Microbiology, 71(1): 1–10.
  • Singh, M., Kumar, A., Singh, R., Pandey, KD. (2017). Endophytic bacteria: A new source of bioactive compounds. Biotechnology, 7(4): 315.
  • SPSS. (2008). IBM SPSS Statistics 17.0 for Windows, Armonk, NY.
  • Sun, ZB., Li, SD., Ren, Q., Xu, JL., Lu, X., Sun, MH. (2020). Biology and applications of Clonostachys rosea. Journal of Applied Microbiology, 129(3): 486-495.
  • Srinivasan, R. (2010). Safer tomato production techniques: A field guide for soil fertility and pest management (Vol. 10, No. 740). AVRDC-World Vegetable Center.
  • ten Hoopen, GM., George, A., Martinez, A., Stirrup, T., Flood, J., Krauss, U. (2010). Compatibility between Clonostachys isolates with a view to mixed inocula for biocontrol. Mycologia, 102(5): 1204–1215.
  • Toral, L., Rodríguez, M., Béjar, V., Sampedro, I. (2018). Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Frontiers in Microbiology, 9, 1315.
  • Usta, M., Güller, A., Demirel, S., Korkmaz, G., Kurt, Z. (2023). New insights into tomato spotted wilt orthotospovirus (TSWV) infections in Türkiye: Molecular detection, phylogenetic analysis, and in silico docking study. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(3): 13245.
  • Vargas Gil, S., Pastor, S., March, GJ. (2009). Quantitative isolation of biocontrol agents Trichoderma spp., Gliocladium spp., and actinomycetes from soil with culture media. Microbiological Research, 164(2): 196–205.
  • Verma, M., Brar, SK., Tyagi, RD., Surampalli, RN., Valero, JR. (2007). Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochemical Engineering Journal, 37(1): 1–20.
  • Vinale, F., Sivasithamparam, K., Ghisalberti, EL., Marra, R., Barbetti, MJ., Li, H., Lorito, M. (2008). A novel role for Trichoderma secondary metabolites in interactions with plants. Physiological and Molecular Plant Pathology, 72(1–3): 80–86.
  • Vukelić, ID., Prokić, LT., Racić, GM., Pešić, MB., Bojović, MM., Sierka, EM., Panković, DM. (2021). Effects of Trichoderma harzianum on photosynthetic characteristics and fruit quality of tomato plants. International Journal of Molecular Sciences, 22(13): 6961. https://doi.org/10.3390/ijms22136961
  • Vural, H., Eşiyok, D., Duman, İ. (2000). Kültür sebzeleri (Sebze yetiştirme). Ege Üniversitesi Ziraat Fakültesi Bahçe Bitkileri Bölümü.
  • Xu, X., Chen, Y., Li, B., Zhang, Z., Qin, G., Chen, T., Tian, S. (2022). Molecular mechanisms underlying multi-level defense responses of horticultural crops to fungal pathogens. Horticulture Research, 9, uhac066.
  • Wang, X., Wang, M., Han, L., Jin, F., Jiao, J., Chen, M., Xue, W. (2021). Novel pyrazole-4-acetohydrazide derivatives potentially targeting fungal succinate dehydrogenase: Design, synthesis, three-dimensional quantitative structure–activity relationship, and molecular docking. Journal of Agricultural and Food Chemistry, 69(33): 9557–9570.
  • Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Schwede, T. (2018). SWISS-MODEL: Homology modeling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. MAP kinases in fungal pathogens. Fungal Genetics and Biology, 31(3), 137–152. https://doi.org/10.1093/nar/gky4272000.
  • Yıldız, M., Özyılmaz, Ü. (2023). Bağda kurşuni küf hastalığı (Botrytis cinerea Pers.)’na karşı antagonist bakterilerle biyolojik mücadele. Türkiye Biyolojik Mücadele Dergisi, 14(2): 121–140.
  • You, J., Zhang, J., Wu, M., Yang, L., Chen, W., Li, G. (2016). Multiple criteria-based screening of Trichoderma isolates for biological control of Botrytis cinerea on tomato. Biological Control, 101, 31-38.
  • Zhang, ZQ., Chen, T., Li, BQ., Qin, GZ., Tian, SP. (2021). Molecular basis of pathogenesis of postharvest pathogenic fungi and control strategy in fruits: Progress and prospect. Molecular Horticulture, 1(1): 1–10.
  • Zheng, L., Gu, X., Xiao, Y., Wang, S., Liu, L., Pan, H., Zhang, H. (2023). Antifungal activity of Bacillus mojavensis D50 against Botrytis cinerea causing postharvest gray mold of tomato. Scientia Horticulturae, 312, 111841.
  • Zhou, C., Sun, X., Fu, W., Li, Z., Cheng, J., Maienfisch, P. (2023). Rational exploration of novel SDHI fungicide through an amide-β-ketonitrile bioisosteric replacement strategy. Journal of Agricultural and Food Chemistry, 71 (14): 5483–5495.

Antagonists for the Control of Botrytis cinerea in Tomatoes: An In Vitro Evaluation and In Silico Screening By Molecular Docking of Possible Inhibitors

Year 2025, Volume: 12 Issue: 3, 870 - 886, 23.07.2025
https://doi.org/10.30910/turkjans.1619273

Abstract

This study was conducted to investigate the antifungal effects of candidate antagonists Clonostachys rosea, Trichoderma harzianum, and Bacillus mojavensis against Botrytis cinerea pathogen and to examine their interactions under in vitro conditions and in silico examine by molecular docking. The effects of candidate antagonist applications on the mycelial growth of B. cinerea M2-1 isolate showed that the most effective isolate was T. harzianum C7-3 (56%) followed by B. mojavensis K193 (32%) and C. rosea C6-4 (26%). When evaluating the interactions between the candidate antagonist isolates, it was determined that T. harzianum and B. mojavensis reduced the mycelial growth of C. rosea compared to the control. In the T. harzianum × B. mojavensis combination, the fungal antagonist’s mycelial growth was inhibited when in contact with the bacterial isolate. Additionally, the effects of candidate antagonists on the root and shoot length of tomato seeds (cv. Super) were measured, and germination percentages were calculated. Clonostachys rosea (3.09 cm) and B. mojavensis (3.57 cm) promoted root development, while B. mojavensis K193 (4.02 cm) enhanced shoot development, and T. harzianum C7-3 improved seed germination percentage (86.7%) compared to the control. The molecular docking findings demonstrated that the combination of ligands from T. harzianum could synergistically enhance antifungal efficacy against B. cinerea by inhibiting or modifying proteins associated with pathogenicity and virulence. Result of in silico study highlighted the necessity for more laboratory research to validate the impact of T. harzianum-derived metabolites on the proteins of B. cinerea and their interactions.

References

  • Akbaba, M., Özaktan, H. (2018). Biocontrol of angular leaf spot disease and colonization of cucumber (Cucumis sativus L.) by endophytic bacteria. Egyptian Journal of Biological Pest Control, 28: 1-10.
  • Alina, SO., Constantinscu, F., Petruţa, CC. (2015). Biodiversity of Bacillus subtilis group and beneficial traits of Bacillus species useful in plant protection. Romanian Biotechnological Letters, 20(5), 10737–10750.
  • Amarouchi, Z., Esmaeel, Q., Sanchez, L., Jacquard, C., Hafidi, M., Vaillant-Gaveau, N., Ait Barka, E. (2021). Beneficial microorganisms to control the gray mold of grapevine: From screening to mechanisms. Microorganisms, 9(7): 1386.
  • Anderson, AC., Stangherlin, S., Pimentel, KN., Weadge, JT., Clarke, AJ. (2022). The SGNH hydrolase family: A template for carbohydrate diversity. Glycobiology, 32(10), 826–848.
  • Blake, C., Christensen, MN., Kovács, ÁT. (2021). Molecular aspects of plant growth promotion and protection by Bacillus subtilis. Molecular Plant-Microbe Interactions, 34(1): 15–25.
  • Boddy, L. (2016). Pathogens of autotrophs. In The fungi (pp. 245–292). Academic Press.
  • Bolivar-Anillo, HJ., González-Rodríguez, VE., Cantoral, JM., García-Sánchez, D., Collado, IG., Garrido, C. (2021). Endophytic bacteria Bacillus subtilis, isolated from Zea mays, as potential biocontrol agent against Botrytis cinerea. Biology, 10(6): 492.
  • Calvo, P., Ormeño-Orrillo, E., Martínez-Romero, E., Zúñiga, D. (2010). Characterization of Bacillus isolates of potato rhizosphere from Andean soils of Peru and their potential PGPR characteristics. Brazilian Journal of Microbiology, 41(4): 899–906.
  • Carillo, P., Woo, SL, Comite, E., El-Nakhel, C., Rouphael, Y., Fusco, GM., Borzacchiello, A., Lanzuise, S., Vinale, F. (2020). Application of Trichoderma harzianum, 6-pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants, 9(6): 771.
  • Cheng, L., Liu, J., Liu, J., Guo, D., Deng, F., Bian Q, et al. (2023). Design, synthesis, antifungal activity and molecular docking of ring-opened pimprinine derivative containing (thio) amide structure. Pest Management Science, 79 (7): 2220–2229.
  • Christopher, DJ., Raj, TS., Rani, SU., Udhayakumar, R. (2010). Role of defense enzymes activity in tomato as induced by Trichoderma virens against Fusarium wilt caused by Fusarium oxysporum f. sp. lycopersici. Journal of Biopesticides, 3(1), 158.
  • Cota, LV., Maffia, LA., Mizubuti, ESG. (2008). Brazilian isolates of Clonostachys rosea: Colonization under different temperature and moisture conditions and temporal dynamics on strawberry leaves. Letters in Applied Microbiology, 46(3): 312–317.
  • Cui, Z., Gao, N., Wang, Q., Ren, Y., Wang, K., Zhu, T. (2015). BcMctA, a putative monocarboxylate transporter, is required for pathogenicity in Botrytis cinerea. Current Genetics, 61(4): 545–553.
  • de Nadal, E., Posas, F. (2009). Multilayered control of gene expression by stress-activated protein kinases. EMBO Journal, 29(4): 4–13.
  • Dean, R., Van Kan, JA., Pretorius, ZA., Hammond‐Kosack, KE., Di Pietro, A., Spanu, PD., Foster, GD. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13(4): 414–430.
  • Demirel, F. (2021). In silico analysis of protein disulfide isomerases in soybean. Journal of Agriculture, 4(1): 48–56.
  • Demirel, S., Güller, A., Usta, M., Kurt, Z., Korkmaz, G. (2024). Coat protein of alfalfa mosaic alfamovirus (AMV) from Türkiye: Genetic inference and in silico docking analysis for potential antiphytoviral purposes. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(1): 13529.
  • Diabankana, RGC., Afordoanyi, DM., Safin, RI., Nizamov, RM., Karimova, LZ., Validov, SZ. (2021). Antifungal properties, abiotic stress resistance, and biocontrol ability of Bacillus mojavensis PS17. Current Microbiology, 78(8): 3124–3132.
  • Earl, AM., Eppinger, M., Fricke, WF., Rosovitz, MJ., Rasko, DA., Daugherty, S., Losick, R., Kolter, R., Ravel, J. (2012). Whole-genome sequences of Bacillus subtilis and close relatives. Journal of Bacteriology, 194(9): 2378–2379.
  • Eken, C., Genç T., S. Tuncer ve Z. Kadıoğlu. (2013). Çilekte kurşuni küf hastalığı etmeni Botrytis cinerea’ya in vitroda fungal antagonistlerin etkisi. Türkiye 5. Organik Tarım Sempozyumu, 25-27 Eylül, Samsun, Türkiye.
  • Elad, Y., Pertot, I., Prado, AMC., Stewart, A. (2016). Plant hosts of Botrytis spp. In Botrytis: The fungus, the pathogen and its management in agricultural systems (pp. 413–486). Springer.
  • Enebe, MC., Babalola, OO. (2019). The impact of microbes in the orchestration of plants’ resistance to biotic stress: A disease management approach. Applied Microbiology and Biotechnology, 103(1): 9–25.
  • Fan, J., Fu, A., Zhang, L. (2019). Progress in molecular docking. Quantitative Biology, 7(1): 83–89.
  • Fiorini, L., Guglielminetti, L., Mariotti, L., Curadi, M., Picciarelli, P., Scartazza, A., Vannacci, G. (2016). Trichoderma harzianum T6776 modulates a complex metabolic network to stimulate tomato cv. Micro-Tom growth. Plant and Soil, 400: 351-366.
  • Fira, D., Dimkić, I., Berić, T., Lozo, J., Stanković, S. (2018). Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285(1): 44–55.
  • Gelmez, C., Müftüoğlu, NM. (2018). Effect of different calcium doses and nitrogen fertilizers on yield and yield characteristic in tomatoes. Journal of Graduate School of Natural and Applied Sciences, 4(2): 134–148.
  • Geng, L., Fu, Y., Peng, X., Yang, Z., Zhang, M., Song, Z. (2022). Biocontrol potential of Trichoderma harzianum against Botrytis cinerea in tomato plants. Biological Control, 174(1): 105019.
  • Grabka, R., d’Entremont, TW., Adams, SJ., Walker, AK., Tanney, JB., Abbasi, PA., Ali, S. (2022). Fungal endophytes and their role in agricultural plant protection against pests and pathogens. Plants, 11(3): 384.
  • Guzmán-Guzmán, P., Kumar, A., de Los Santos-Villalobos, S., Parra-Cota, FI., Orozco-Mosqueda, MDC., Fadiji, AE. (2023). Trichoderma species: Our best fungal allies in the biocontrol of plant diseases—A review. Plants, 12(3): 432.
  • Hahn, M. (2014). The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. Journal of Chemical Biology, 7(4): 133–141.
  • Hammad, M., Guillemette, T., Alem, M., Bastide, F., Louanchi, M. (2021). First report of three species of Trichoderma isolated from the rhizosphere in Algeria and the high antagonistic effect of Trichoderma brevicompactum to control grey mould disease of tomato. Egyptian Journal of Biological Pest Control, 31(1): 85.
  • Han, Z., Ghanizadeh, H., Zhang, H., Li, X., Li, T., Wang, Q., Liu, J., Wang, A. (2022). Clonostachys rosea promotes root growth in tomato by secreting auxin produced through the tryptamine pathway. Journal of Fungi, 8(11): 1166.
  • Hang, NTT., Oh, SO., Kim, GH., Hur, JS., Koh, YJ. (2005). Bacillus subtilis S1-0210 as a biocontrol agent against Botrytis cinerea in strawberries. The Plant Pathology Journal, 21 (1): 59-63.
  • Kesimci, TG., Dönmez, MF. (2022). Determining of the antagonist effects of bacteria againts Botrytis cinerea in strawberry under in vitro conditions. Yuzuncu Yil University Journal of the Institute of Natural and Applied Sciences, 27 (3): 535-547.
  • Khalil, AMA., Abdelaziz, AM., Khaleil, MM., Hashem, AH. (2021). Fungal endophytes from leaves of Avicennia marina growing in semi-arid environment as a promising source for bioactive compounds. Letters in Applied Microbiology, 72: 263–274.
  • Kiesewalter, HT., Lozano-Andrade, CN., Maróti, G., Snyder, D., Cooper, VS., Jørgensen, TS., Kovács, ÁT. (2020). Complete genome sequences of 13 Bacillus subtilis soil isolates for studying secondary metabolite diversity. Microbiology Resource Announcements, 9(2): 10-1128.
  • Krauss, U., Ten Hoopen, M., Rees, R., Stirrup, T., Argyle, T., George, A, ... Casanoves, F. (2013). Mycoparasitism by Clonostachys byssicola and Clonostachys rosea on Trichoderma spp. from cocoa (Theobroma cacao) and implication for the design of mixed biocontrol agents. Biological Control, 67(3): 317-327.
  • Kredics, L., Antal, Z., Manczinger, L., Szekeres, A., Kevei, F., Nagy, E. (2003). Influence of environmental parameters on Trichoderma strains with biocontrol potential. Food Technology and Biotechnology, 41(1): 37-42.
  • Kumar, M. Ashraf S. (2017). Role of Trichoderma spp. as a biocontrol agent of fungal plant pathogens. Probiotics and Plant Health, 497-506.
  • Kumar, SM., Chowdappa, P., Krishna, V. (2015). Development of seed coating formulation using consortium of Bacillus subtilis OTPB1 and Trichoderma harzianum OTPB3 for plant growth promotion and induction of systemic resistance in field and horticultural crops. Indian Phytopathology, 68(1): 25-31.
  • Lahlali, R., Ezrari, S., Radouane, N., Kenfaoui, J., Esmaeel, Q., El Hamss H., ... Barka, EA. (2022). Biological control of plant pathogens: A global perspective. Microorganisms, 10(3): 596.
  • Li, F., Ghanizadeh, H., Song, W., Miao, S., Wang, H., Chen, X., ... Wang, A. (2023). Combined use of Trichoderma harzianum and Clonostachys rosea to manage Botrytis cinerea infection in tomato plants. European Journal of Plant Pathology, 167(4): 637-650.
  • Mamiev, MS., Khakimov, AA., Zuparov, MA., Rakhmonov, UN. (2020). Effectiveness of different fungicides in controlling Botrytis grey mould of tomato. In IOP Conference Series: Earth and Environmental Science 614 (1), December, p. 012112, IOP Publishing.
  • Martínez-Absalón, S., Rojas-Solís, D., Hernández-León, R., Prieto-Barajas, C., Orozco-Mosqueda, MDC., Peña-Cabriales, JJ., .. Santoyo, G. (2014). Potential use and mode of action of the new strain Bacillus thuringiensis UM96 for the biological control of the grey mould phytopathogen Botrytis cinerea. Biocontrol Science and Technology, 24(12), 1349-1362.
  • Meng, F., Lv, R., Cheng, M., Mo, F., Zhang, N., Qi H, ... Wang, A. (2022). Insights into the molecular basis of biocontrol of Botrytis cinerea by Clonostachys rosea in tomato. Scientia Horticulturae, 291: 110547.
  • Mónaco, C., Dal Bello, G., Rollán, MC., Ronco, L., Lampugnani, G., Arteta, N., ... Stocco, M. (2009). Biological control of Botrytis cinerea on tomato using naturally occurring fungal antagonists. Archives of Phytopathology and Plant Protection, 42(8): 729-737.
  • Moriwaki, A., Kubo, E., Arase, S., Kihara, J. (2006). Disruption of SRM1, a mitogen-activated protein kinase gene, affects sensitivity to osmotic and ultraviolet stressors in the phytopathogenic fungus Bipolaris oryzae. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol Lett. 257:253-261.
  • Mouekouba, LDO., Zhang, L., Guan, X., Chen, X., Chen, H., Zhang, J., ... Wang, A. (2014). Analysis of Clonostachys rosea-induced resistance to tomato gray mold disease in tomato leaves. PLoS One, 9(7): e102690.
  • Muniroh, MS., Nusaibah, SA., Vadamalai, G., Siddique, Y. (2019). Proficiency of biocontrol agents as plant growth promoters and hydrolytic enzyme producers in Ganoderma boninense infected oil palm seedlings. Current Plant Biology, 20, 100116.
  • Nawrocka, J., Szymczak, K., Maćkowiak, A., Skwarek-Fadecka, M., Małolepsza, U. (2022). Determination of reactive oxygen or nitrogen species and novel volatile organic compounds in the defense responses of tomato plants against Botrytis cinerea induced by Trichoderma virens TRS 106. Cells, 11(19), 3051.
  • Özden, E. (2019). The Effect of pre-sown treatments on seed viability and physiology in tomato. In: AGROFOOD-International Conference on Agronomy and Food Science and Technology, 20-21 Haziran, İstanbul, Türkiye, 394-401.
  • Pandit, MA., Kumar, J., Gulati, S., Bhandari, N., Mehta, P., Katyal, R., Kaur, J. (2022). Major biological control strategies for plant pathogens. Pathogens, 11(2): 273.
  • Pettersen, EF., Goddard, TD., Huang, CC., Couch, GS., Greenblatt, DM., Meng, EC., et al. (2004). UCSF Chimera—avisualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13):1605–12. Plaza, V., Lagües, Y., Carvajal, M., Pérez-García, LA., Mora-Montes, HM., Canessa, P., Larrondo, LF., Castillo, L. (2015). bcpmr1 encodes a P-type Ca2+/Mn2+-ATPase mediating cell-wall integrity and virulence in the phytopathogen Botrytis cinerea. Fungal Genetics and Biology, 76: 36–46
  • Poveda, J., Barquero, M., González-Andrés, F. (2020). Insight into the microbiological control strategies against Botrytis cinerea using systemic plant resistance activation. Agronomy, 10(11): 1822.
  • Rahila, R., Harish, S., Kalpana, K., Anand, G., Arulsamy, M., Kalaivanan, R. (2023). Antifungal metabolites of Streptomyces chrestomyceticus STR-2 inhibits Magnaporthe oryzae, the incitant of rice blast. Current Microbiology, 80(4): 107.
  • Risoli, S., Cotrozzi, L., Sarrocco, S., Nuzzaci, M., Pellegrini, E., Vitti, A. (2022). Trichoderma-induced resistance to Botrytis cinerea in Solanum species: A meta-analysis. Plants, 11(2): 180.
  • Roca-Couso, R., Flores-Félix, JD., Rivas, R. (2021). Mechanisms of action of microbial biocontrol agents against Botrytis cinerea. Journal of Fungi (Basel, Switzerland), 7(12): 1045. https://doi.org/10.3390/jof7121045
  • Saddek, D., Messgo-Moumene, S., Chemat-Djenni, Z., Bendifallah, L., Bencheikh, K. (2020). Antagonism of isolates of Trichoderma spp. against Botrytis cinerea Pers., the agent of gray rot of tomato (Lycopersicum esculentum Mill.) under greenhouse conditions. Journal of Fundamental and Applied Sciences, 12(2): 583–606.
  • Sancaktaroğlu, S., Yıldırım, B., Ekici, K., Demirel, F. (2023). Characterization of essential oil and in silico modeling perspectives of thyme (Thymus eigii M. Zohary et P.H. Davis) jalas species. Iğdır Üniversitesi Tarım Bilimleri Dergisi, 1(2): 52–60.
  • Saraiva, RM., Czymmek, KJ., Borges, AV., Caires, NP., Maffia, LA. (2015). Confocal microscopy study to understand Clonostachys rosea and Botrytis cinerea interactions in tomato plants. Biocontrol Science and Technology, 25(1): 56–71.
  • Saravanakumar, K., Yu, C., Dou, K., Wang, M., Li, Y., Chen, J. (2016). Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall-degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. cucumerinum. Biological Control, 94: 37–46.
  • Saravanakumar, K., Lu, Z., Xia, H., Wang, M., Sun, J., Wang, S., .Chen, J. (2018). Triggering the biocontrol of Botrytis cinerea by Trichoderma harzianum through inhibition of pathogenicity and virulence-related proteins. Biological Control, 123: 53–62.
  • Sati, D., Joshi, T., Pandey, SC., Pande, V., Mathpal, S., Chandra, S., Samant, M. (2022). Identification of putative elicitors from plant root exudates responsible for PsoR activation in plant-beneficial Pseudomonas spp. by docking and molecular dynamics simulation approaches to decipher plant–microbe interaction. Frontiers in Plant Science, 13, 875494.
  • Schaeffer, HJ., Weber, MJ. (1999). Mitogen-activated protein kinases: Specific messages from ubiquitous messengers. Molecular and Cellular Biology, 19(4), 2435–2444.
  • Senkovs, M., Nikolajeva, V., Makarenkova, G., Petrina, Z. (2021). Influence of Trichoderma asperellum and Bacillus subtilis as biocontrol and plant growth-promoting agents on soil microbiota. Annals of Microbiology, 71(1): 1–10.
  • Singh, M., Kumar, A., Singh, R., Pandey, KD. (2017). Endophytic bacteria: A new source of bioactive compounds. Biotechnology, 7(4): 315.
  • SPSS. (2008). IBM SPSS Statistics 17.0 for Windows, Armonk, NY.
  • Sun, ZB., Li, SD., Ren, Q., Xu, JL., Lu, X., Sun, MH. (2020). Biology and applications of Clonostachys rosea. Journal of Applied Microbiology, 129(3): 486-495.
  • Srinivasan, R. (2010). Safer tomato production techniques: A field guide for soil fertility and pest management (Vol. 10, No. 740). AVRDC-World Vegetable Center.
  • ten Hoopen, GM., George, A., Martinez, A., Stirrup, T., Flood, J., Krauss, U. (2010). Compatibility between Clonostachys isolates with a view to mixed inocula for biocontrol. Mycologia, 102(5): 1204–1215.
  • Toral, L., Rodríguez, M., Béjar, V., Sampedro, I. (2018). Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Frontiers in Microbiology, 9, 1315.
  • Usta, M., Güller, A., Demirel, S., Korkmaz, G., Kurt, Z. (2023). New insights into tomato spotted wilt orthotospovirus (TSWV) infections in Türkiye: Molecular detection, phylogenetic analysis, and in silico docking study. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(3): 13245.
  • Vargas Gil, S., Pastor, S., March, GJ. (2009). Quantitative isolation of biocontrol agents Trichoderma spp., Gliocladium spp., and actinomycetes from soil with culture media. Microbiological Research, 164(2): 196–205.
  • Verma, M., Brar, SK., Tyagi, RD., Surampalli, RN., Valero, JR. (2007). Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochemical Engineering Journal, 37(1): 1–20.
  • Vinale, F., Sivasithamparam, K., Ghisalberti, EL., Marra, R., Barbetti, MJ., Li, H., Lorito, M. (2008). A novel role for Trichoderma secondary metabolites in interactions with plants. Physiological and Molecular Plant Pathology, 72(1–3): 80–86.
  • Vukelić, ID., Prokić, LT., Racić, GM., Pešić, MB., Bojović, MM., Sierka, EM., Panković, DM. (2021). Effects of Trichoderma harzianum on photosynthetic characteristics and fruit quality of tomato plants. International Journal of Molecular Sciences, 22(13): 6961. https://doi.org/10.3390/ijms22136961
  • Vural, H., Eşiyok, D., Duman, İ. (2000). Kültür sebzeleri (Sebze yetiştirme). Ege Üniversitesi Ziraat Fakültesi Bahçe Bitkileri Bölümü.
  • Xu, X., Chen, Y., Li, B., Zhang, Z., Qin, G., Chen, T., Tian, S. (2022). Molecular mechanisms underlying multi-level defense responses of horticultural crops to fungal pathogens. Horticulture Research, 9, uhac066.
  • Wang, X., Wang, M., Han, L., Jin, F., Jiao, J., Chen, M., Xue, W. (2021). Novel pyrazole-4-acetohydrazide derivatives potentially targeting fungal succinate dehydrogenase: Design, synthesis, three-dimensional quantitative structure–activity relationship, and molecular docking. Journal of Agricultural and Food Chemistry, 69(33): 9557–9570.
  • Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Schwede, T. (2018). SWISS-MODEL: Homology modeling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. MAP kinases in fungal pathogens. Fungal Genetics and Biology, 31(3), 137–152. https://doi.org/10.1093/nar/gky4272000.
  • Yıldız, M., Özyılmaz, Ü. (2023). Bağda kurşuni küf hastalığı (Botrytis cinerea Pers.)’na karşı antagonist bakterilerle biyolojik mücadele. Türkiye Biyolojik Mücadele Dergisi, 14(2): 121–140.
  • You, J., Zhang, J., Wu, M., Yang, L., Chen, W., Li, G. (2016). Multiple criteria-based screening of Trichoderma isolates for biological control of Botrytis cinerea on tomato. Biological Control, 101, 31-38.
  • Zhang, ZQ., Chen, T., Li, BQ., Qin, GZ., Tian, SP. (2021). Molecular basis of pathogenesis of postharvest pathogenic fungi and control strategy in fruits: Progress and prospect. Molecular Horticulture, 1(1): 1–10.
  • Zheng, L., Gu, X., Xiao, Y., Wang, S., Liu, L., Pan, H., Zhang, H. (2023). Antifungal activity of Bacillus mojavensis D50 against Botrytis cinerea causing postharvest gray mold of tomato. Scientia Horticulturae, 312, 111841.
  • Zhou, C., Sun, X., Fu, W., Li, Z., Cheng, J., Maienfisch, P. (2023). Rational exploration of novel SDHI fungicide through an amide-β-ketonitrile bioisosteric replacement strategy. Journal of Agricultural and Food Chemistry, 71 (14): 5483–5495.
There are 85 citations in total.

Details

Primary Language English
Subjects Phytopathology
Journal Section Research Article
Authors

Tuba Genç Kesimci 0000-0003-2022-0193

Mustafa Akbaba 0000-0002-7029-9461

Serap Demirel 0000-0002-1877-0797

Publication Date July 23, 2025
Submission Date January 15, 2025
Acceptance Date April 15, 2025
Published in Issue Year 2025 Volume: 12 Issue: 3

Cite

APA Genç Kesimci, T., Akbaba, M., & Demirel, S. (2025). Antagonists for the Control of Botrytis cinerea in Tomatoes: An In Vitro Evaluation and In Silico Screening By Molecular Docking of Possible Inhibitors. Turkish Journal of Agricultural and Natural Sciences, 12(3), 870-886. https://doi.org/10.30910/turkjans.1619273