Evaluation of pathogenic variation among Rhizoctonia solani isolates infecting different crops and potential biocontrol agents

Year 2024, Volume: 64 Issue: 4, 29 - 40

Abdelhak Rhouma , Lobna Hajji-hedfi , Pravin Babasaheb Khaire , Abdulnabi Matrood

https://doi.org/10.16955/bitkorb.1507155

Abstract

Rhizoctonia solani is an important broad-spectrum fungal pathogen that infects over 200 plant species including tomato, melon, and watermelon. This study evaluated the pathogenicity of various R. solani isolates (Rs26, Rs94, Rs13, Rs57, and Rs123) and the efficacy of biological agents (Trichoderma harzianum, T. viride, Metarhizium sp., Gliocladium sp.) under laboratory and greenhouse conditions for eco-friendly disease management. The results of the pathogenicity assay confirmed the varying aggressiveness of the isolates, with Rs94 and Rs13 causing the most severe disease in watermelon (disease severity (DS) = 3.80 and 3.83, disease severity index (DSI) = 90.43% and 95.75%, respectively). Similarly, isolate Rs26 displayed the highest pathogenicity in tomatoes (DS = 3.84; DSI = 94.86%). Melon exhibited high susceptibility across all isolates, with consistently high DS and DSI values exceeding 2.59 and 80.97%, respectively. Subsequent in vitro and in vivo assays demonstrated the antifungal potential of all tested agents against R. solani isolates. Notably, Trichoderma spp. displayed the most consistent and significant inhibition (mycelial growth reduction 82.97%-94.67%), with T. harzianum demonstrating superior performance. Greenhouse trials confirmed the effectiveness of T. harzianum as a preventative treatment, enhancing plant enzyme activity [peroxidase = 4.97-5.29 units g-1 ml-1 min-1 for tomato and watermelon, respectively; catalase = 99.93-101.22 units g-1 ml-1 min-1 for watermelon and melon, respectively] and significantly reducing disease severity index (DSI < 12.43%). These findings highlight the potential of T. harzianum as a sustainable and eco-friendly strategy for managing R. solani damping-off disease in tomato, melon, and watermelon crops.

Keywords

Damping-off disease, Trichoderma spp., tomato, melon, pathogenicity, watermelon

Farklı ürün türlerini enfekte eden Rhizoctonia solani izolatları arasındaki patojenik varyasyonun ve potansiyel biyokontrol ajanlarının değerlendirilmesi

Abstract

Rhizoctonia solani, domates, kavun ve karpuz dahil olmak üzere 200'den fazla bitki türünü enfekte eden önemli ve geniş spektrumlu bir fungal patojendir. Bu çalışmada, farklı R. solani izolatlarının (Rs26, Rs94, Rs13, Rs57 ve Rs123) patojenitesi ve çevre dostu hastalık yönetimi için Trichoderma harzianum, T. viride, Metarhizium sp., Gliocladium sp. gibi biyolojik ajanların etkinliği laboratuvar ve sera koşullarında değerlendirilmiştir. Patojenite testlerinin sonuçları, izolatların değişen virülensini doğrulamıştır. Rs94 ve Rs13 izolatları karpuzda en ciddi hastalığa neden olmuştur (hastalık şiddeti (HS)= 3.80 ve 3.83, hastalık şiddeti indeksi (HSİ)= %90.43 ve %95.75). Benzer şekilde, Rs26 izolatı domateste en yüksek patojenisiteyi sergilemiştir (HS= 3.84; HSİ= %94.86). Kavun, tüm izolatlara karşı yüksek hassasiyet göstermiş olup, sürekli olarak 2.59'dan yüksek HS ve %80.97' yi aşan HSİ değerleri kaydedilmiştir. Daha sonra yapılan in vitro ve in vivo denemeler, test edilen tüm ajanların R. solani izolatlarına karşı antifungal potansiyelini ortaya koymuştur. Özellikle Trichoderma spp., en tutarlı ve anlamlı inhibisyonu göstermiştir (miselyal büyüme azalması %82.97-%94.67). Bu konuda en iyi performansı ise T. harzianum göstermiştir. Sera denemeleri, T. harzianum'un önleyici bir tedavi olarak etkinliğini doğrulamış, bitki enzim aktivitesini artırmış (peroksidaz = domates ve karpuz için sırasıyla 4.97-5.29 birim g-1 ml-1 dk-1; katalaz = karpuz ve kavun için sırasıyla 99.93-101.22 birim g-1 ml-1 dk-1) ve hastalık şiddeti indeksini önemli ölçüde azaltmıştır (HSİ < %12.43). Bu bulgular, T. harzianum'un domates, kavun ve karpuz bitkilerinde R. solani fide yanıklığı hastalığının yönetimi için sürdürülebilir ve çevre dostu bir strateji olarak kullanım potansiyelini vurgulamaktadır.

Keywords

Fide yanıklık hastalığı, Trichoderma spp., domates, kavun, patojenisite, karpuz

References

• Abbas A., Ali A., Hussain A., Ali A., Alrefaei A.F., Naqvi S.A.H., Rao M.J., Mubeen I., Farooq T., Olmez F., 2023. Assessment of genetic variability and evolutionary relationships of Rhizoctonia solani inherent in legume crops. Plants, 12, 2515. https://doi.org/10.3390/plants12132515
• Abbas A., Jiang D., Fu Y., 2017. Trichoderma spp. as antagonist of Rhizoctonia solani. Journal of Plant Pathology and Microbiology, 8, 402. https://doi.org/10.4172/2157-7471.1000402
• Abdelghany M.M.A., Kurikawa M., Watanabe M., Matsui H., Yamamoto M., Ichinose Y., Toyoda K., Kouzai Y., Noutoshi Y., 2022. Surveillance of pathogenicity of Rhizoctonia solani Japanese isolates with varied anastomosis groups and subgroups on Arabidopsis thaliana. Life, 12 (1), 76. https://doi.org/10.3390/life12010076
• Abd-El-Khair H., Khalifa R.Kh.M., Haggag K.H.E., 2011. Effect of Trichoderma species on damping off diseases incidence, some plant enzymes activity and nutritional status of bean plants. Journal of American Science, 7(1), 156-167.
• Agrios G.N., 1988. Plant pathology. New York: Academic Press, 803 p.
• Albastawisi E.M., Kotan R., 2024. Bacterial biocontrol agents against diseases caused by Rhizoctonia solani in sugar beet. Indian Phytopathology, 77, 211-217. https://doi.org/10.1007/s42360-023-00697-8
• Ali H.H., Taha K.K., 2016. Biological control of tomato damping-off disease using Trichoderma harzianum and Bacillus subtilis. Zanco Journal of Pure and Applied Sciences, 28, 12-19. https://doi.org/10.21271/ZJPAS.28.3.3
• Almaghasla M.I., El-Ganainy S.M., Ismail A.M., 2023. Biological activity of four Trichoderma species confers protection against Rhizoctonia solani, the causal agent of cucumber damping-off and root rot diseases. Sustainability, 15 (9), 7250. https://doi.org/10.3390/su15097250
• Amer M.A., Abou-El-Seoud II., 2008. Mycorrhizal fungi and Trichoderma harzianum as biocontrol agents for suppression of Rhizoctonia solani damping off disease of tomato. Communications in Agricultural and Applied Biological Sciences, 73 (2), 217-232.
• Asaduzzaman M., Alam M.J., Islam M.M., 2010. Effect of Trichoderma on seedgermination and seedling parameters of chili. Journal of Science Foundation, 8 (1-2), 141-150. https://doi.org/10.3329/jsf.v8i1-2.14637
• Baghani F., Rahnama K., Aghajani M.A., Dehghan M.A., 2012. Biological control of fusarium head blight (Fusarium graminearum) by application of three native Trichoderma species in field. Journal of Plant Production Research, 19 (2), 123-139.
• Bailey B.A., Bae H., Strem M.D., Crozier J., Thomas S.E., Samuels G.J., Vinyard B.T., Holmes K.A., 2008. Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biological Control, 46 (1), 24-35. https://doi.org/10.1016/j.biocontrol.2008.01.003
• Ban G., Shamsul A., Macquin M., 2022. Efficacy of Trichoderma harzianum against Fusarium oxysporum and Rhizoctonia solani on bean and tomato plants. Annals of Tropical Research, 44 (1), 30-45. https://doi.org/10.32945/atr4413.2022
• Behiry S., Soliman S.A., Massoud M.A., Abdelbary M., Kordy A.M., Abdelkhalek A., Heflish A., 2023. Trichoderma pubescens elicit induced systemic resistance in tomato challenged by Rhizoctonia solani. Journal of Fungi, 9 (2), 167. https://doi.org/10.3390/jof9020167
• Biam M., Majumder D., 2019. Biocontrol efficacy of Trichoderma isolates against tomato damping off caused by Pythium spp. And Rhizoctonia solani (Kuhn.). International Journal of Chemical Studies, 7 (3), 81-89.
• Brindhadevi S., Thavapriya T., Tanusri C., Thangaguruvu K., Tharun P.N., Durga Nandhini M., Jeevitha S., 2023. In vitro evaluation of bio agents against Rhizoctonia solani causing root rot of tomato. The Pharma Innovation Journal, 12 (6), 160-162.
• Brunner K., Zeilinger S., Ciliento R., Woo S.L., Lorito M., Kubicek C.P., Mach R.L., 2005. Improvement of the fungal biocontrol agent Trichoderma atroviride to enhance both antagonism and induction of plant systemic disease resistance. Application of Environmental Microbiology, 71 (7), 3959-3965. https://doi.org/10.1128/AEM.71.7.3959-3965.2005
• Cai F., Yu G., Wang P., Wei Z., Fu L., Shen Q., Chen W., 2013. Harzianolide, a novel plantgrowth regulator and systemic resistance elicitor from Trichoderma harzianum. Plant Physiology and Biochemistry, 73, 106-113. https://doi.org/10.1016/j.plaphy.2013.08.011
• Canpolat S., Tülek S., 2019. Orta Anadolu Bölgesi’nde yaprağı yenen sebzelerde görülen fungal hastalıkların belirlenmesi. Plant Protection Bulletin, 59 (3), 39-46. https://doi.org/10.16955/bitkorb.527754
• Canpolat S., Woodward S., Kurbetli İ., 2023. Molecular and pathological characterization of the isolates of Rhizoctonia spp. associated with dry bean (Phaseolus vulgaris) in Türkiye. Journal of Plant Pathology, 105 (2), 837-848. https://doi.org/10.1007/s42161-023-01377-2
• Carling D.E., Pope E.J., Brainard K.A., Carter D.A., 1999. Characterization of mycorrhizal isolates of Rhizoctonia solani from an orchid, including AG-12, a new anastomosis group. Phytopathology, 89, 942-946. https://doi.org/10.1094/PHYTO.1999.89.10.942
• Devi U.G., Rajendraprasad M., Vidyasagar B., Rao S.R.K., 2017. Biological control of tomato damping off caused by Pythium debaryanum. International Journal of Chemical Studies, 5 (5), 447-452.
• Dubey S.C., Bhavani R., Singh B., 2011. Integration of soil application and seed treatment formulations of Trichoderma species for management of wet root rot of mung bean caused by Rhizoctonia solani. Pest Management Science, 67 (9), 1163-1168. https://doi.org/10.1002/ps.2168
• Dubey S.C., Tripathi A., Upadhyay B.K., 2012. Molecular diversity analysis of Rhizoctonia solani isolates infecting various pulse crops in different agro-ecological regions of India. Folia Microbiologica, 57, 513-524. https://doi.org/10.1007/s12223-012-0165-y
• Eken C., Demir D., Uysal G., Çalışkan S., Sevindik E., Çağlayan K., 2024. Isolation, identification, and pathogenicity of Rhizoctonia spp. recovered from soil samples of the greenhouse tomato growing area of the west mediterranean region, Türkiye. Journal of Phytopathology, 172 (2). https://doi.org/10.1111/jph.13297
• Elsheshtawi A., El-Gazzar T., AbouTabl A., Ebid M., 2012. Effect of biocontrol agents and natural plant extracts and oils on the growth of Rhizoctonia solani, a pathogen on tomato, in vitro. Journal of Plant Protection and Pathology, 3 (1), 1-12. https://doi.org/10.21608/jppp.2012.83676
• Erper I., Ozer G., Kalendar R., Avci S., Yildirim E., Alkan M., Turkkan M., 2021. Genetic diversity and pathogenicity of Rhizoctonia spp. isolates associated with red cabbage in Samsun (Turkey). Journal of Fungi, 7 (3), 234. https://doi.org/10.3390/jof7030234
• Gajera H.P., Katakpara Z.A., Patel S.V., Golakiya B.A., 2016. Antioxidant defense response induced by Trichoderma viride against Aspergillus niger Van Tieghemcausing collar rot in groundnut (Arachis hypogaea L.). Microbial Pathogenesis, 91, 26-34. https://doi.org/10.1016/j.micpath.2015.11.010
• 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
• Hanson L.D., 2000. Reduction of Verticillium wilt symptoms in cotton following seed treatment with Trichoderma virens. The Journal of Cotton Science, 4, 224-231.
• Howell C.R., 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Disease, 87 (1), 4-10. https://doi.org/10.1094/PDIS.2003.87.1.4
• Huang X., Chen L., Ran W., Shen Q., Yang X., 2011. Trichoderma harzianum strain SQR-T37 and its bio-organic fertilizer could control Rhizoctonia solani damping-off disease in cucumber seedlings mainly by the mycoparasitism. Applied Microbiology and Biotechnology, 91, 741-755. https://doi.org/10.1007/s00253-011-3259-6
• Kaveh H., Jartoodeh S.V., Aruee H., Mazhabi M., 2011. Would Trichoderma affect seed germination and seedling quality of two muskmelon cultivars, Khatooniand Qasri and increase their transplanting success. Journal of Biodiversity and Environmental Science, 5 (15), 169-175.
• Kobori N.N., Mascarin G.M., Jackson M.A., Schisler D.A., 2015. Liquid culture production of microsclerotia and submerged conidia by Trichoderma harzianum active against damping-off disease caused by Rhizoctonia solani. Fungal Biology, 119, 179-190. https://doi.org/10.1016/j.funbio.2014.12.005
• Lewis J.A., Lumsden R.D., 2001. Biocontrol of damping-off of greenhouse-grown crops caused by Rhizoctonia solani with a formulation of Trichoderma spp. Crop Protection, 20 (1), 49-56. https://doi.org/10.1016/S0261-2194(00)00052-1
• Li C., Guo Z., Zhou S., Han Q., Zhang M., Peng Y., Hsiang T., Chen X., 2021. Evolutionary and genomic comparisons of hybrid uninucleate and nonhybrid Rhizoctonia fungi. Communications Biology, 4, 201. https://doi.org/10.1038/s42003-021-01724-y
• 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
• Mishra D.S., Sinha A.P., 2000. Plant growth promoting activity of some fungal and bacterial agents on rice seed germination and seedling growth. Tropical Agriculture, 77 (3), 188-191.
• Mohamed B.F.F., Sallam N.M.A., Alamri S.A.M., Abo-Elyousr K.A.M., Mostafa Y.S., Hashem M., 2020. Approving the biocontrol method of potato wilt caused by Ralstonia solanacearum (Smith) using Enterobacter cloacae PS14 and Trichoderma asperellum T34. Egyptian Journal of Biological Pest Control, 30, 61. https://doi.org/10.1186/s41938-020-00262-9
• Motesharrei Z.S., Salimi H., 2014. Biocontrol characteristics of Trichoderma spp. against Fusarium in Iran. Middle East Journal of Scientific Research, 22 (8), 1122-1126.
• Mustafa A.A., Abass M.H., Awad K.M., 2021. Responses of tomato to Rhizoctonia solani infection under the salinity stress. International Journal of Agriculture and Biology, 26 (6), 707-716. https://doi.org/10.17957/ijab/15.1886
• Naeimi S., Okhovvat S.M., Javan-Nikkhah M., Vágvölgyi C., Khosravi V., Kredics L., 2010. Biological control of Rhizoctonia solani AG1-1A, the causal agent of rice sheath blight with Trichoderma strains. Phytopathologia Mediterranea, 49 (3), 287-300. http://www.jstor.org/stable/26458654
• Naqvi S.A.H., Abbas A., Farhan M., Kiran R., Hassan Z., Mehmood Y., Ali A., Ahmed N., Hassan M.Z., Alrefaei A.F., 2024. Unveiling the genetic tapestry: exploring Rhizoctonia solani AG-3 anastomosis groups in potato crops across borders. Plants, 13 (5), 715. https://doi.org/10.3390/plants13050715
• Okon O.G., Rhouma A., Ismaila U., Matrood A.A.A., Hajji-Hedfi L., 2023. Biological control of fruit rot of postharvest orange (Citrus aurantium) by aqueous plant extracts. Indian Journal of Agricultural Sciences, 93, 1243-1247. https://doi.org/10.56093/ijas.v93i11.141146
• Oyarbide F., Osterrieth M.L., Cabello M., 2001. As a Trichoderma koningii biomineralizing fungus agent of calcium oxalate crystals in typical Argiudolls of the Los Padres Lake natural reserve (Buenos Aires, Argentina). Microbiological Research, 156 (2), 113-119. https://doi.org/10.1078/0944-5013-00083
• Ozan S., Maden S., 2004. Root and crown rot and wilt of tomatoes caused by fungal diseases in Ankara province. Plant Protection Bulletin, 44 (1), 105-120. https://dergipark.org.tr/en/pub/bitkorb/issue/3671/48773
• Ozan S., Aşkın A., 2006. Studies on fungal diseases of protected vegetable areas in central Anatolia region. Plant Protection Bulletin, 46 (1), 65-74. https://dergipark.org.tr/en/pub/bitkorb/issue/3673/48779
• Paula Júnior T.J., Rotter C., Hau B., 2007. Effects of soil moisture and sowing depth on the development of bean plants grown in sterile soil infested by Rhizoctonia solani and Trichoderma harzianum. European Journal of Plant Pathology, 119, 193-202. https://doi.org/10.1007/s10658-007-9161-5
• 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
• Porto M., Ambrósio M., Nascimento S., Cruz B., Torres T., 2019. Interaction of Fusarium solani, Macrophomina phaseolina and Rhizoctonia solani as root rot pathogens of Cucumis melo. Summa Phytopathologica, 45 (4), 355-360. https://doi.org/10.1590/0100-5405/182687
• Rehman S.U., Lawrence R., Kumar E.J., Badri Z.A., 2011. Comparative efficacy of Trichoderma viride, T. harzianum and carbendazim against damping-off disease of cauliflower caused by Rhizoctonia solani Kuehn. Journal of Biopesticides, 5 (1), 23-27. https://doi.org/10.57182/jbiopestic.5.1.23-27
• Rhouma A., Hajji-Hedfi L., El Amine Kouadri M., Chihani-Hammas N., Babasaheb Khaire P., 2024. Investigating plant growth promoting and antifungal potential of Metarhizium spp. against Fusarium wilt in tomato. Nova Hedwigia, 119 (1-2), 117-139. https://doi.org/10.1127/nova_hedwigia/2024/0958
• Ruiz-Cisneros M.F., Ornelas-Paz J.J., Olivas-Orozco G.I., Acosta-Muñiz C.H., Sepulveda-Ahumada D.R., Pérez-Corral D.A., Rios-Velasco C., Salas-Marina M.A., Fernández-Pavía S.P., 2018. Effect of Trichoderma spp. and phytopathogenic fungi on plant growth and tomato fruit quality. Revista Bio Ciencias 6, e541. https://doi.org/10.15741/revbio.06.e541
• Segarra G., Casanova E., Avilés M., Trillas I., 2010. Trichoderma asperellum Strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for Iron. Microbial Ecology, 59, 141-149. https://doi.org/10.1007/s00248-009-9545-5
• Shalaby T.A., Taha N., El-Beltagi H.S., El-Ramady H., 2022. Combined application of Trichoderma harzianum and Paclobutrazol to control root rot disease caused by Rhizoctonia solani of tomato seedlings. Agronomy, 12 (12), 3186. https://doi.org/10.3390/agronomy12123186
• Smolinska U., Kowalska B., Oskiera M., 2007. The effectivity of Trichoderma strains in the protection of cucumber and lettuce against Rhizoctonia solani. Journal of Fruit and Ornamental Plant Research, 67 (1), 81-93. https://doi.org/10.2478/v10032-007-0033-5
• Sreenivasaprasad S., Manibhushanrao K., 1990. Biocontrol potential of fungal antagonists Gliocladium virens and Trichoderma longibrachiatum. Journal of Plant Diseases and Protection, 97 (3), 570-579. https://www.jstor.org/stable/43385867
• Thakur N., Tripathi A., 2015. Biological management of damping-off, buckeye rot and Fusarium wilt of tomato (cv. Solan lalima) under mid-hill conditions of Himachal Pradesh. Agricultural Sciences, 6, 535-544. https://doi.org/10.4236/as.2015.65053
• Yang Y., Zhang J., Yan J., Zhao L., Luo L., Li C., Yang G., 2024. Effects of chemical and biological fungicide applications on sexual sporulation of Rhizoctonia solani AG-3 TB on tobacco. Life, 14 (3), 404. https://doi.org/10.3390/life14030404
• Yücel S., Ay T., Çolak A., 2008. Effect of Trichoderma harzianum rifai KRL AG2 to control root rot disease (Rhizoctonia solani, Fusarium solani) of cucumber in protected crops. Plant Protection Bulletin, 48 (2), 41-47. https://dergipark.org.tr/en/pub/bitkorb/issue/3676/48798