Trichoderma koningii ve Rhizophagus irregularis'in domateste Fusarium solgunluk hastalığına karşı etkinliğinin belirlenmesi

Öz

Bu çalışmada, sera koşullarında domateste Fusarium solgunluk hastalığının kimyasal mücadelesine alternatif olarak çevre dostu Trichoderma koningii ve Rhizophagus irregularis'in potansiyeli araştırılmıştır. Araştırma, T. koningii ve R. irregularis’in nasıl etkileşime girdiğine ve bitki büyümesi ve hastalık direnci üzerindeki etkilerine odaklanmıştır. T. koningii tek başına hastalık şiddetini Fusarium oxysporum f. sp. lycopersici (FOL) ile enfekte edilmiş kontrol grubuna kıyasla önemli ölçüde azaltmıştır (DS = 0.83; DSI = %29.33). Ancak, en etkili koruma T. koningii ve R. irregularis’in birlikte kullanımından elde edilmiş (DS = 0.33; DSI = %14.33) ve sağlıklı kontrollerle karşılaştırılabilir bir seviyeye ulaşılmıştır. Bu kombine uygulama sadece etkili hastalık direnci göstermekle kalmamış, aynı zamanda en yüksek klorofil içeriğini de göstermiştir (Chl a = 5.62 mg g-1 Taze Ağırlık; Chl b = 3.11 mg g-1 Taze Ağırlık; Chl T = 8.74 mg g-1 Taze Ağırlık), bu da FOL enfeksiyonunun neden olduğu klorofil bozunmasına karşı koymada daha güçlü bir yeteneğe işaret etmektedir. Ek olarak, T. koningii ve R. irregularis ile birlikte aşılanan domates bitkileri en güçlü antioksidan tepkiyi sergileyerek, antioksidan enzimlerinin (süperoksit dismutaz = 46.17 birim g-1 ml-1 dk-1, peroksidaz aktivitesi = 5.66 birim g-1 ml-1 dk-1 ve katalaz aktivitesi = 104.42 birim g-1 ml-1 dk-1) ve toplam fenolik içeriğinin (3.14 mg g-1) belirgin şekilde daha yüksek olduğunu göstermiştir. Bu bulgular, T. koningii ve R. irregularis'in birlikte uygulanmasının, T. koningii veya R. irregularis’in tek başına kullanılmasına kıyasla, domateste Fusarium solgunluk hastalığının yönetimi ve genel bitki sağlığının geliştirilmesi açısından daha etkili ve çevre dostu bir strateji olma potansiyeline sahip olduğunu göstermektedir.

Anahtar Kelimeler

• arbusküler mikorizal fungus
• Solanum lycopersicum
• Fusarium oxysporum f. sp. lycopersici
• sera denemesi

Determination of the efficacy of Trichoderma koningii and Rhizophagus irregularis against Fusarium wilt disease in tomato

Öz

This study investigated the potential of Trichoderma koningii and Rhizophagus irregularis as environmentally friendly as an alternative to chemical control for Fusarium wilt disease in tomato under greenhouse conditions. The research focused on how these T. koningii and R. irregularis interacted and their impact on plant growth and disease resistance. T. koningii alone significantly reduced disease severity (DS = 0.83; DSI = 29.33%) compared to the control group infected with Fusarium oxysporum f. sp. lycopersici (FOL). However, the most effective protection came from combining both T. koningii and R. irregularis (DS = 0.33; DSI = 14.33%), achieving a level comparable to healthy controls. This combined treatment not only displayed superior disease resistance but also showed the highest chlorophyll content (Chl a = 5.62 mg g-1 Fresh Weight; Chl b = 3.11 mg g-1 Fresh Weight; Chl T = 8.74 mg g-1 Fresh Weight), indicating a stronger ability to counteract the chlorophyll degradation caused by FOL infection. Furthermore, tomato plants co-inoculated with T. koningii and R. irregularis exhibited the most robust antioxidant response, evident in significantly higher activities of antioxidant enzymes (superoxide dismutase = 46.17 units g-1 ml-1 min-1, peroxidase activity = 5.66 units g-1 ml-1 min-1, and catalase activity = 104.42 units g-1 ml-1 min-1) and total phenolic content (3.14 mg g-1). These findings suggest that the combined application of T. koningii and R. irregularis has the potential to be a more effective and environmentally friendly strategy for managing Fusarium wilt disease and promoting overall plant health in tomato compared to using either T. koningii or R. irregularis alone.

Anahtar Kelimeler

• arbuscular mycorrhizal fungi
• Solanum lycopersicum
• Fusarium oxysporum f.sp. lycopersici
• greenhouse assay

Kaynakça

1. Abbaspour H., Saeidi-Sar S., Afshari H., Abdel-Wahhab M.A., 2012. Tolerance of mycorrhiza infected pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. Journal of Plant Physiology, 169 (7), 704-709. https://doi.org/10.1016/j.jplph.2012.01.014
2. Adriano-Anaya, M.L., Salvador-Figueroa M., Ocampo J.A. García-Romera I., 2006. Hydrolytic enzyme activities in maize (Zea mays) and sorghum (Sorghum bicolor) roots inoculated with Gluconacetobacter diazotrophicus and Glomus intraradices. Soil Biology and Biochemistry, 38 (5), 879-86. https://doi.org/10.1016/j.soilbio.2005.08.004
3. Andrino A., Guggenberger G., Kernchen S., Mikutta R., Sauheitl L., Boy J., 2021. Production of organic acids by arbuscular mycorrhizal fungi and their contribution in the mobilization of phosphorus bound to iron oxides. Frontiers in Plant Science, 12, 661842. https://doi.org/10.3389/fpls.2021.661842
4. Bisht A., Garg N., 2024. Harnessing the role of arbuscular mycorrhizae in arresting nodular senescence by modulating osmolyte synthesis and ascorbate-glutathione pool in cadmium stressed pigeon pea. Plant Growth Regulation, 102, 409-427. https://doi.org/10.1007/s10725-023-01069-y
5. Brizuela A.M., Gálvez L., Arroyo J.M., Sánchez S., Palmero D., 2023. Evaluation of Trichoderma spp. on Fusarium oxysporum f. sp. asparagi and Fusarium wilt control in Asparagus crop. Plants, 12 (15), 2846. https://doi.org/10.3390/plants12152846
6. Burke D.J., Carrino-Kyker S.R., 2021. The influence of mycorrhizal fungi on rhizosphere bacterial communities in forests. Forest Microbiology, 1, 257-275. https://doi.org/10.1016/B978-0-12-822542-4.00017-6
7. Chen J., Zhang H.Q., Zhang X.L., Tang M., 2020. Arbuscular mycorrhizal symbiosis mitigates oxidative injury in black locust under salt stress through modulating antioxidant defence of the plant. Environmental and Experimental Botany, 175, 104034. https://doi.org/10.1016/j.envexpbot.2020.104034
8. Chen S., Jin W., Liu A., Zhang S., Liu D., Wang F., Lin X., He C., 2013. Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Scientia Horticulturae, 160, 222-229. https://doi.org/10.1016/j.scienta.2013.05.039

9. Dehariya K., Shukla A., Sheikh I.A., Vyas D., 2015. Trichoderma and arbuscular mycorrhizal fungi based biocontrol of Fusarium udum Butler and their growth promotion effects on pigeon pea. Journal of Agricultural Science and Technology, 17 (2), 505-517. http://jast.modares.ac.ir/article-23-2021-en.html
10. Delaeter M., Magnin-Robert M., Randoux B., Lounès-Hadj Sahraoui A., 2024. Arbuscular mycorrhizal fungi as biostimulant and biocontrol agents: a review. Microorganisms, 12 (7), 1281. https://doi.org/10.3390/microorganisms12071281
11. Diagne N., Ngom M., Djighaly P.I., Fall D., Hocher V., Svistoonoff S., 2020. Roles of arbuscular mycorrhizal fungi on plant growth and performance: importance in biotic and abiotic stressed regulation. Diversity, 12 (10), 370. https://doi.org/10.3390/d12100370
12. Dodd J.C., Boddington C.L., Rodríguez A., Gonzales-Chaves C., Mansur I., 2000. Mycelium of arbuscular mycorrhizal fungi (AMF) from different genera: form, function and detection. Plant and Soil, 226, 131-151. https://doi.org/10.1023/A:1026574828169
13. Egberongbe H.O., Akintokun A.K., Babalola O.O., Bankole M.O., 2010. The effect of Glomus mosseae and Trichoderma harzianum on proximate analysis of soybean (Glycine max (L.) Merrill.) seed grown in sterilized and unsterilized soil. Journal of Agricultural Extension Rural Development, 2 (4), 54-58. https://doi.org/10.5897/JAERD.9000071
14. Elbekkay M., Hamza H., Neily M.H., Djebali N., Ferchichi A., 2021. Characterization of watermelon local cultivars from Southern Tunisia using morphological traits and molecular markers. Euphytica, 217, 74. https://doi.org/10.1007/s10681-021-02809-9
15. Emmett B.D., Lévesque-Tremblay V., Harrison M.J. 2021. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME Journal, 15 (8), 2276-2288. https://doi.org/10.1038/s41396-021-00920-2
16. FAO., 2024. Food and Agriculture Organization. Available at: https://www.fao.org/faostat/en/
17. Guzmán-Guzmán P., Kumar A., de los Santos-Villalobos S., Parra-Cota F.I., Orozco-Mosqueda M.d.C., Fadiji A.E., Hyder S., Babalola O.O., 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
18. Hajji-Hedfi L., Rhouma A., Al-Judaibi A.A. Hajlaoui H., Hajlaoui F., Azeem A.M.A., 2024. Valorization of Capsicum annuum seed extract as an antifungal against Botrytis cinerea. Waste and Biomass Valorization, 15, 2559-2573. https://doi.org/10.1007/s12649-023-02322-1
19. Hajji-Hedfi L., Rhouma A., Hajlaoui H., Hajlaoui F., Rebouh N.Y., 2023. Understanding the influence of applying two culture filtrates to control gray mold disease (Botrytis cinerea) in tomato. Agronomy, 13 (7), 1774. https://doi.org/10.3390/agronomy13071774
20. He A.L., Liu J., Wang X.H., Zhang Q., Song W., Chen J., 2019. Soil application of Trichoderma asperellum GDFS1009 granules promotes growth and resistance to Fusarium graminearum in maize. Journal of Integrative Agriculture, 18 (3), 599-606. https://doi.org/10.1016/S2095-3119(18)62089-1
21. Jiang F., Zhang L., Zhou J., George T.S., Feng G., 2021. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytologist, 230, 304-315. https://doi.org/10.1111/nph.17081
22. Jmal Z., Labidi S., Dalpe Y., Slim S., Lounès-Hadj Sahraoui A., Ben Jeddi F., 2015. Diversité de champignons mycorhiziens arbusculaires d’un bas fond halomorphe en Tunisie. Journal of New Sciences, 18 (2), 648-657.
23. Kakabouki I., Mavroeidis A., Tataridas A., Kousta A., Efthimiadou A., Karydogianni S., Katsenios N., Roussis I., Papastylianou P., 2021. Effect of Rhizophagus irregularis on growth and quality of Cannabis sativa seedlings. Plants, 10 (7), 1333. https://doi.org/10.3390/plants10071333
24. Kalamulla R., Karunarathna S.C., Tibpromma S., Galappaththi M.C.A., Suwannarach N., Stephenson S.L., Asad S., Salem Z.S., Yapa N., 2022. Arbuscular mycorrhizal fungi in sustainable agriculture. Sustainability, 14 (19), 12250. https://doi.org/10.3390/su141912250
25. Keinath A.P., Coolong T.W., Lanier J.D., Ji P., 2019. Managing Fusarium wilt of watermelon with delayed transplanting and cultivar resistance. Plant Disease, 103 (1), 44-50. https://doi.org/10.1094/PDIS-04-18-0709-RE
26. Keinath A.P., DuBose V.B., Katawczik M.M., Katawczik M.M., Wechter W.P., 2020. Identifying races of Fusarium oxysporum f. sp. niveum in south Carolina recovered from watermelon seedlings, plants, and field soil. Plant Disease, 104 (9), 2481-2488. https://doi.org/10.1094/PDIS-11-19-2385-RE
27. Khalediyan N., Weisany W., Schenk P.M., 2021. Arbuscular mycorrhizae and rhizobacteria improve growth, nutritional status and essential oil production in Ocimum basilicum and Satureja hortensis. Industrial Crops and Products, 160, 113163. https://doi.org/10.1016/j.indcrop.2020.113163
28. Khaliq A., Perveen S., Alamer K.H., Zia Ul Haq M., Rafique Z., Alsudays I.M., Althobaiti A.T., Saleh M.A., Hussain S., Attia H., 2022. Arbuscular mycorrhizal fungi symbiosis to enhance plant-soil interaction. Sustainability, 14 (13), 7840. https://doi.org/10.3390/su14137840
29. Kubiak A., Wolna-Maruwka A., Pilarska A.A., Niewiadomska A., Piotrowska-Cyplik A., 2023. Fungi of the Trichoderma genus: future perspectives of benefits in sustainable agriculture. Applied Sciences, 13 (11), 6434. https://doi.org/10.3390/app13116434
30. Li Y.Q., Sun R.Y., Yu J., Saravanakumar K., Chen, J., 2016. Antagonistic and biocontrol potential of Trichoderma asperellum ZJSX5003 against the maize stalk rot pathogen Fusarium graminearum. Indian Journal of Microbiology, 56, 318-327. https://doi.org/10.1007/s12088-016-0581-9
31. Liu Q.M., Chen X., Meng X.H., 2017. Development of a new type of biological organic fertilizer and its effect on the growth promotion of tomato. Chinese Journal of Applied Ecology, 28, 3314-3322. https://doi.org/10.13287/j.1001-9332.201710.039
32. Matrood A.A.A., Rhouma A., 2021. Evaluating eco-friendly botanicals as alternatives to synthetic fungicides against the causal agent of early blight of Solanum melongena. Journal of Plant Diseases and Protection, 128, 1517-1530. https://doi.org/10.1007/s41348-021-00530-2
33. Matrood A.A.A., Rhouma A., 2022. Bioprotection of Cucumis melo from Alternaria leaf spot by Glomus mosseae and Trichoderma harzianum. Tropicultura, 40 (2), 2295-8010. https://doi.org/10.25518/2295-8010.2075
34. Merina Prem Kumari S., Prabina B.J., 2019. Protection of tomato, Lycopersicon esculentum from wilt pathogen, Fusarium oxysporum f.sp. lycopersici by arbuscular mycorrhizal fungi, Glomus sp. International Journal of Current Microbiology and Applied Sciences, 8 (4), 1368-1378. https://doi.org/10.20546/ijcmas.2019.804.159
35. Mota I., Sánchez-Sánchez J., Pedro L.G., Sousa M.J., 2020. Composition variation of the essential oil from Ocimum basilicum L. cv. Genovese Gigante in response to Glomus intraradices and mild water stress at different stages of growth. Biochemical Systematics and Ecology, 90, 104021. https://doi.org/10.1016/j.bse.2020.104021
36. Mousa M.A.A, Abo-Elyousr K.A.M., Abdel Alal A.M.K., Alshareef N.O., 2021. Management Fusarium wilt disease in tomato by combinations of Bacillus amyloliquefaciens and peppermint oil. Agronomy, 11 (12), 2536. https://doi.org/10.3390/agronomy11122536
37. Müller L.M., Flokova K., Schnabel E., Sun X., Fei Z., Frugoli J., Bouwmeester H.J., Harrison M.J., 2019. A CLE–SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza. Nature Plants, 5, 933-939. https://doi.org/10.1038/s41477-019-0501-1
38. Nicolás C., Calvo-Polanco M., Poveda J., Alonso-Ramírez A., Ascaso J., Arbona V., Hermosa R., 2024. The presence of arbuscular mycorrhizal fungi in the rhizosphere of transgenic rapeseed overexpressing a Trichoderma Thkel1 gene improves plant development and yield. Agriculture, 14 (6), 851. https://doi.org/10.3390/agriculture14060851
39. Ozan S., Maden S., 2004. Ankara ili domates ekiliş alanlarında solgunluk ve kök ve kökboğazı çürüklüğüne neden olan fungal hastalık etmenleri. Bitki Koruma Bülteni (Plant Protection Bulletin), 44 (1-4), 105-120.
40. Ozan S., Aşkın A., 2006. Orta Anadolu bölgesi örtü altı sebze alanlarında görülen fungal hastalıklar üzerinde çalışmalar. Bitki Koruma Bülteni (Plant Protection Bulletin), 46, (1-4), 65-75.
41. Paliwoda D., Mikiciuk G., 2020. Use of rhizosphere microorganisms in plant production-a review study. Journal of Ecological Engineering, 21 (8), 292-310. https://doi.org/10.12911/22998993/126597
42. Pan S., Wang Y., Qiu Y,. Chen D., Zhang L., Ye C., Guo H., Zhu W., Chen A., Xu G., Zhang Y., Bai Y., Hu S., 2020. Nitrogen-induced acidification, not N-nutrient, dominates suppressive N effects on arbuscular mycorrhizal fungi. Global Change Biology, 26 (11), 6568-6580. https://doi.org/10.1111/gcb.15311
43. Popoola A.R., Durosomo A.H., Afolabi C.G., Idehen E.O., 2015. Regeneration of somaclonal variants of tomato (Solanum lycopersicum L.) for resistance to Fusarium wilt. Journal of Crop Improvement, 29 (5), 636-649. https://doi.org/10.1080/15427528.2015.1066287
44. Porteous-Álvarez A.J., Fernández-Marcos A., Ramírez-Lozano D., Mayo-Prieto S., Cardoza R.E., Gutiérrez S., Casquero P.A., 2023. Native Trichoderma isolates from soil and rootstock to Fusarium spp. control and growth promotion of Humulus lupulus L. plantlets. Agriculture, 13 (3), 720. https://doi.org/10.3390/agriculture13030720
45. Ramesh R., Singh N.P., 2017. Field evaluation of talc formulation of Trichoderma for the management of Fusarium wilt in watermelon. Indian Phytopathology, 70 (1), 75-79. https://doi.org/10.24838/ip.2017.v70.i1.49000
46. Rhouma A., Mougou I., Bedjaoui H., Rhouma H., Matrood A.A.A., 2021. Ecology in Chott Sidi Abdel Salam oasis, southeastern Tunisia: cultivated vegetation, fungal diversity and livestock population. Journal of Coastal Conservations, 25, 52. https://doi.org/10.1007/s11852-021-00837-0
47. Rhouma A., Mehaoua M.S., Mougou I., Rhouma H., Shah K.K., Bedjaoui H., 2023. Combining melon varieties with chemical fungicides for integrated powdery mildew control in Tunisia. European Journal of Plant Pathology, 165, 189-201. https://doi.org/10.1007/s10658-022-02599-3
48. Rhouma A., Hajji-Hedfi L., Alsayd Bouqellah N., Babasaheb Khaire P., Dali S., Bargougui O., Khlif A., Al-Ani L.K.T., 2024. Uniting the role of entomopathogenic fungi against Rhizoctonia solani JG Kühn, the causal agent of cucumber damping-off and root rot diseases. Phyton-International Journal of Experimental Botany, 93 (11), 2857-2881. https://doi.org/10.32604/phyton.2024.057591
49. Robinson R.W., Decker-Walters D.S., 1997. Cucurbits. CAB International, New York, 226 p.
50. Shi J., Wang X., Wang E., 2023. Mycorrhizal symbiosis in plant growth and stress adaptation: from genes to ecosystems. Annual Review of Plant Biology, 74, 569-607. https://doi.org/10.1146/annurev-arplant-061722-090342
51. Spagnoletti F., Carmona M., Gómez N.E., Chiocchio V., Lavado R.S., 2017. Arbuscular mycorrhiza reduces the negative effects of M. phaseolina on soybean plants in arsenic-contaminated soils. Applied Soil Ecology, 121, 41-47. https://doi.org/10.1016/j.apsoil.2017.09.019
52. Taribuka J., Wibowo A., Widyastuti S.M., Sumardiyono C., 2017. Potency of six isolates of biocontrol agents endophytic Trichoderma against Fusarium wilt on banana. Journal of Degraded and Mining Lands Management, 4 (2), 723-731. https://doi.org/10.15243/jdmlm.2017.042.723
53. Tyśkiewicz R., Nowak A., Ozimek E., Jaroszuk-Scisel J., 2022. Trichoderma: The current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. International Journal of Molecular Sciences, 23 (4), 2329. https://doi.org/10.3390/ijms23042329
54. Wahab A., Muhammad M., Munir A., Abdi G., Zaman W., Ayaz A., Khizar C., Reddy S.P.P., 2023. Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants, 12 (17), 3102. https://doi.org/10.3390/plants12173102
55. Wang Y., Li Y., He P., Chen J., Lamikanra O., Lu J., 1995. Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species. Vitis, 34 (3), 159-164. https://doi.org/10.5073/vitis.1995.34.159-164
56. Wang Y.Y., Yin Q.S., Qu Y., 2017. Arbuscular mycorrhiza-mediated resistance in tomato against Cladosporium fulvum -induced mould disease. Journal of Phytopathology, 166 (1), 67-74.
57. Zhang F.G., Xu X.X., Huo Y.Q., Xiao Y., 2019. Trichoderma-inoculation and mowing synergistically altered soil available nutrients, rhizosphere chemical compounds and soil microbial community, potentially driving alfalfa growth. Frontiers in Microbiology, 9, 3241. https://doi.org/10.3389/fmicb.2018.03241
58. Zhang Y., Xiao J.L., Yang K., Wang Y., Tian Y., Liang Z., 2022. Transcriptomic and metabonomic insights into the biocontrol mechanism of Trichoderma asperellum M45a against watermelon Fusarium wilt. PLOS ONE, 17 (8), e0272702. https://doi.org/10.1371/journal.pone.0272702