Domates (Solanum lycopersicium L.) Bitkisinde, Verticillium Solgunluğu (Verticillium Dahliae Kleb.) ve Erken Yanıklığı [Alternaria solani (Ell. Ve G. Martin) Sor.] Hastalıklarına Karşı Clonostachys rosea (Sch.) Schroers ve Samuels’nin Etkisinin Belirlenmesi

Abstract

Bu çalışmada, domates yetiştiriciliğinde sorun olan ve önemli ekonomik kayıplara neden olan Verticillium solgunluğu (Verticillium dahliae) ve Erkenci Yaprak Yanıklığı (Alternaria solani) hastalıklarına karşı Clonostachys rosea'nin etkinliğinin belirlenmesi amaçlanmıştır. In vitro çalışmalarda fungal biyokontrol ajanı C. rosea'nin A. solani ve V. dahliae üzerinde etkili olduğu ve misel gelişimini baskıladığı belirlenmiştir. In vivo çalışmalarında ise C. rosea buğday tanelerine bulaştırılarak, patojen inokulasyonlarının öncesinde ve sonrasında bitkilere 20 g, 30 g ve 40 g uygulama dozlarında uygulanmıştır. Daha sonra V. dahliae stoklarından 2 mm çapında diskler alınarak bitkinin kök bölgesine uygulanmıştır. A. solani ise bitkilerin yeşil kısımlarına el spreyi ile püskürtülerek 1x106 konidia/ml oranında inokule edilmiştir. V. dahliae kontrol bitkilerinde %76.0 hastalık şiddetine neden olurken, domates bitkilerinde buğday tanelerine aşılanan C. rosea izolatının 20g, 30g ve 40g uygulama dozlarının hastalık şiddeti sırasıyla %58.3, %55.3 ve %25.3 olarak belirlenmiştir. A. solani x C. rosea x domates patosisteminde ise hastalık şiddeti kontrolde %96.6 oranındayken, C. rosea'nin 20g, 30g ve 40g uygulama dozları sırasıyla %63.3, %43.6 ve %46.6 olarak belirlenmiştir. C. rosea'nin patojen baskılama oranları en yüksek değer A. solani için 30 g (%54.8) ve V. dahliae için 40 g (%66.6) doz olarak tespit edilmiştir. Çalışmada ayrıca C. rosea'nin bitki büyümesi üzerindeki etkileri de belirlenmeye çalışılmıştır. Elde edilen bulgulara göre, C. rosea domates bitkisinin morfolojik gelişimine olumlu etki yapmıştır.

Keywords

• Domates
• Biyolojik kontrol
• Clonostachys rosea
• Alternaria solani
• Verticillum dahliae

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

Abstract

The effectiveness of Clonostachys rosea against Verticillium wilt (Verticillium dahliae) and early blight (Alternaria solani) diseases, as the two most important problems in tomato cultivation with significant economic losses, was determined. It was determined that C. rosea was effective on A. solani and V. dahliae and suppressed mycelial growth. Also, the C. rosea on wheat grains inoculated to plants at 20 g, 30 g, and 40 g concentrations before and after pathogens inoculation. Then, fungal discs (2 mm in diameter) from V. dahliae growing colonies were inoculated on the host plant root zone. A. solani was also inoculated (1x106 conidia ml-1) by spraying the foliar parts of the plants. Results showed that V. dahliae caused 76.0% disease severity in control plants, while the disease severity indices were 58.3%, 55.3%, and 25.3% at 20 g, 30 g, and 40 g C. rosea application, respectively. In A. solani x C. rosea treatments, the disease severities were determined as 96.6%, 63.3%, 43.6% and 46.6% in control, 20 g, 30 g, and 40 g application of C. rosea, respectively. The pathogen suppression rates by C. rosea at 30g application dose was 54.8% against A. solani and at 40 g application dose was 66.6% against V. dahliae. The effects of C. rosea on plant growth parameters were also determined. Results showed that C. rosea had a positive effect on the morphological parameters in tomato plants.

Keywords

• Tomato
• Biological control
• Clonostachys rosea
• Alternaria solani
• Verticillium dahliae.

References

1. Acharya, B., Ingram, T. W., Oh, Y., Adhikari, T. B., Dean, R. A., & Louws, F. J. (2020). Opportunities and challenges in studies of host-pathogen interactions and management of Verticillium dahliae in tomatoes. Plants, 9(11), 16-22.
2. Agamy, R., Alamri, S., Moustafa, M. F., & Hashem, M. (2013). Management of tomato leaf spot caused by Alternaria tenuissima Wiltshire using salicylic acid and agrileen. International Journal of Agriculture and Biology, 15(2), 266-276.
3. Ait-Rahou, Y., Ait-El-Mokhtar, M., Anli, M., Boutasknit, A., Ben-Laouane, R., Douira, A., & Meddich, A. (2021). Use of mycorrhizal fungi and compost for improving the growth and yield of tomato and its resistance to Verticillium dahliae. Archives of Phytopathology and Plant Protection, 54(13-14), 665-690.
4. Amin, F., Razdan, V. K., Mohiddin, F. A., Bhat, K. A., & Sheikh, P. A. (2010). Effect of volatile metabolites of Trichoderma species against seven fungal plant pathogens in-vitro. Journal of Phytology, 2(10).
5. Azcón-Aguilar, C., & Barea, J. M. (1997). Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza, 6(6), 457-464.
6. Bainier, G. (1907). Mycothéque de l'école de Pharmacie. XI. Paecilomyces, genre nouveau de Mucédinées. Bulletin Trimestrielle de la Societe de Mycologie Française, 23, 26-27.
7. Benouzza, S., Bellahcene, M., & Fortas, Z. (2021). Biocontrol of Verticillium dahliae by native Trichoderma strains isolated from Algeria. MYCOPATH, 18(2), 59-70.
8. Bletsos, F., Thanassoulopoulos, C., & Roupakias, D. (2003). Effect of grafting on growth, yield, and Verticillium wilt of eggplant. HortScience, 38(2), 183-186. Bora, T. (2002). Bitki hastalıklarıyla biyolojik savaşta gelişmeler ve Türkiye’de durum. Türkiye, 5, 4-7.

9. Boyno, G. (2019). Van’da Domates Alanlarından İzole Edilen Alternaria solani (Ell. ve G. Martin) Sor.’nin Biyolojik Mücadele Olanaklarının Belirlenmesi (yüksek lisans tezi, basılmamış). Van Yüzüncü Yıl Üniversitesi Fen Bilimleri Enstitüsü, Van.
10. Boyno, G., Demir, S. & Danesh, Y. R. (2022). Effects of some biological agents on the growth and biochemical parameters of tomato plants infected with Alternaria solani (Ellis & Martin) Sorauer. Eur J Plant Pathol 162, 19–29.
11. Boyno, G., Demir, S., & Akköprü, A. (2020). Domateste Alternaria solani (Ell. & G. Martin) Sor.’ye Karşı Bazı Endofit Bakterilerin Etkisi. Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi, 6(3), 469-477.
12. Chatterton, S., Jayaraman, J., & Punja, Z. K. (2008). Colonization of cucumber plants by the biocontrol fungus Clonostachys rosea f. catenulata. Biological Control, 46(2), 267-278.
13. Chowdappa, P., Kumar, S. M., Lakshmi, M. J., & Upreti, K. K. (2013). Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biological control, 65(1), 109-117.
14. Demir, S. (2005). Using of arbuscular mycorrhizal fungi (AMF) for biocontrol of soil-borne fungal pathogens. Biological control of plant diseases: current concepts, 124-138.
15. Demir, S., Şensoy, S., Ocak, E., Tüfenkci, Ş., Durak, E. D., Erdinc, C., & Ünsal, H. (2015). Effects of arbuscular mycorrhizal fungus, humic acid, and whey on wilt disease caused by Verticillium dahliae Kleb. in three solanaceous crops. Turkish Journal of Agriculture and Forestry, 39(2), 300-309.
16. Devanathan, M., & Ramanujam, K. (1995). Evaluation of fungicides for the management of early blight of tomato caused by Alternaria solani. Madras Agricultural Journal, 82(3), 228-229.
17. Erdoğan, O., Şener, K., & Göre, M. E. (2014). Pamukta Verticillium Solgunluk Hastalığı Etmeni Verticillium dahliae Kleb. ile Farklı İnokulasyon Metotları Üzerinde Çalışmalar. Türk Tarım ve Doğa Bilimleri Dergisi, 1(2), 188-193.
18. Erwin, D. C., Tsoti, S. D., & Khan, R. A. (1976). Reduction of severity of Verticillium wilt of cotton by the growth retardant tributyl (5-chloro-2-thienyl methyl) phosphonium chloride. Phytopathology, 66, 106-110.
19. Faheed, F. A., Abd-Elaah, G. A., & Mazen, A. (2005). Alleviation of disease effect on tomato plants by heat shock and salicylic acid infected with Alternaria solani. Int J Agric Biol, 7, 783-789.
20. FAO, 2020. FAOSTAT–Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#home. Erişim Tarihi:15.10.2021.
21. 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), 1-17.
22. Flores, W., Chico, J., & Cerna, L. (2015). Actividad antagónica in vitro de Clonostachys rosea sobre Fusarium oxysporum, Alternaria solani y Botrytis cinérea. REBIOL, 35(1), 34-42.
23. Foolad, M. R., Ntahimpera, N., Christ, B. J., & Lin, G. Y. (2000). Comparison of field, greenhouse, and detached-leaflet evaluations of tomato germ plasm for early blight resistance. Plant disease, 84(9), 967-972.
24. Fritz, M., Jakobsen, I., Lyngkjær, M. F., Thordal-Christensen, H., & Pons-Kühnemann, J. (2006). Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza, 16(6), 413-419.
25. Gannibal, P. B., Orina, A. S., Mironenko, N. V., & Levitin, M. M. (2014). Differentiation of the closely related species, Alternaria solani and A. tomatophila, by molecular and morphological features and aggressiveness. European Journal of Plant Pathology, 139(3), 609-623.
26. Goh, Y. K., Marzuki, N. F., Tuan Pa, T. N. F., Goh, T. K., Kee, Z. S., Goh, Y. K., & Goh, K. J. (2020). Biocontrol and Plant-Growth-Promoting Traits of Talaromyces apiculatus and Clonostachys rosea Consortium against Ganoderma Basal Stem Rot Disease of Oil Palm. Microorganisms, 8(8), 1138.
27. Gómez-Lama Cabanás, C., Ruano-Rosa, D., Legarda, G., Pizarro-Tobías, P., Valverde-Corredor, A., Triviño, J. C., ... & Mercado-Blanco, J. (2018). Bacillales members from the olive rhizosphere are effective biological control agents against the defoliating pathotype of Verticillium dahliae. Agriculture, 8(7), 90.
28. Grigolli, J. F. J., Kubota, M. M., Alves, D. P., Rodrigues, G. B., Cardoso, C. R., Silva, D. J. H. D., & Mizubuti, E. S. G. (2011). Characterization of tomato accessions for resistance to early blight. Crop Breeding and Applied Biotechnology, 11, 174-180.
29. Harman, G. E. (2006). Overview of mechanisms and uses of Trichoderma spp. Phytopathology, 96(2), 190-194.
30. Jensen, B., Knudsen, I. M., 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.
31. Jensen, J. S., Cusini, M., Gomberg, M., & Moi, H. (2016). 2016 European guideline on Mycoplasma genitalium infections. Journal of the European Academy of Dermatology and Venereology, 30(10), 1650-1656.
32. Jones, J. B., Jones, J. P., Stall, R. E., & Zitter, T. A. (1991). Infectious antifungal. Plant physiology, 108, 17-27.
33. Karthika, S., Varghese, S., & Jisha, M. S. (2020). Exploring the efficacy of antagonistic rhizobacteria as native biocontrol agents against tomato plant diseases. 3 Biotech, 10(7), 1-17.
34. Keinath, A. P., Fravel, D. R., & Papavizas, G. C. (1991). Potential of Gliocladium roseum for biocontrol of Verticillium dahliae. Phytopathology, 81(6), 644-648.
35. Kosawang, C., Karlsson, M., Vélëz, H., Rasmussen, P. H., Collinge, D. B., Jensen, B., & Jensen, D. F. (2014). Zearalenone detoxification by zearalenone hydrolase is important for the antagonistic ability of Clonostachys rosea against mycotoxigenic Fusarium graminearum. Fungal Biology, 118(4), 364-373.
36. Krauss, U., & Soberanis, W. (2001). Biocontrol of cocoa pod diseases with mycoparasite mixtures. Biological control, 22(2), 149-158.
37. Krauss, U., Martínez, A., Hidalgo, E., ten HOOPEN, M., & Arroyo, C. (2002). Two-step liquid/solid state scaled-up production of Clonostachys rosea. Mycological Research, 106(12), 1449-1454.
38. Lahlali, R., & Peng, G. (2014). Suppression of clubroot by Clonostachys rosea via antibiosis and induced host resistance. Plant Pathology, 63(2), 447-455.
39. 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.
40. Morandi, D. (1996). Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant and soil, 185(2), 241-251.
41. Murphy, J. F., Reddy, M. S., Ryu, C. M., Kloepper, J. W., & Li, R. (2003). Rhizobacteria-mediated growth promotion of tomato leads to protection against Cucumber mosaic virus. Phytopathology, 93(10), 1301-1307.
42. Naik, S. C., Narute, T. K., Narute, T. T., & Khaire, P. B. (2020). In-vitro efficacy of biocontrol agents against Alternaria solani (Early Blight of Tomato). Journal of Pharmacognosy and Phytochemistry, 9(5), 550-552.
43. Nygren, K., Dubey, M., Zapparata, A., Iqbal, M., Tzelepis, G. D., Durling, M. B., & 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.
44. Poveda, J., & Baptista, P. (2021). Filamentous fungi as biocontrol agents in olive (Olea europaea L.) diseases: mycorrhizal and endophytic fungi. Crop Protection, 105672.
45. Robb, J. (2007). Verticillium tolerance: resistance, susceptibility, or mutualism?. Botany, 85(10), 903-910.
46. 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.
47. Rodríguez, M. A., Cabrera, G., Gozzo, F. C., Eberlin, M. N., & Godeas, A. (2011). Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist: mechanisms involved and potential as a biocontrol agent. Journal of Applied Microbiology, 110(5), 1177-1186.
48. Royse, D. J., & Ries, S. M. (1978). The influence of fungi isolated from peach twigs on the pathogenicity of Cytospora cincta. Phytopathology, 68(4), 603-607.
49. 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, 72-79.
50. Schoneberg, T., Liebscher, I., Luo, R., Monk, K. R., & Piao, X. (2015). Tethered agonists: a new mechanism underlying adhesion G protein-coupled receptor activation. Journal of Receptors and Signal Transduction, 35(3), 220-223.
51. 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(2), 365-385.
52. Shaban, M., Miao, Y., Ullah, A., Khan, A. Q., Menghwar, H., Khan, A. H., & Zhu, L. (2018). Physiological and molecular mechanism of defense in cotton against Verticillium dahliae. Plant physiology and biochemistry, 125, 193-204.
53. Shinde, B. A., Dholakia, B. B., Hussain, K., Aharoni, A., Giri, A. P., & Kamble, A. C. (2018). WRKY1 acts as a key component improving resistance against Alternaria solani in wild tomato, Solanum arcanum Peralta. Plant biotechnology journal, 16(8), 1502-1513.
54. Silva-Valderrama, I., Toapanta, D., Miccono, M. D. L. A., Lolas, M., Díaz, G. A., Cantu, D., & Castro, A. (2021). Biocontrol potential of grapevine endophytic and rhizospheric fungi against trunk pathogens. Frontiers in microbiology, 11, 3311.
55. 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.
56. 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 Reports, 5(1), 1-10.
57. Sun, Z. B., Wang, Q., Zhang, J., Jiang, W. Z., Li, S. D., Ma, G. Z., & Sun, M. H. (2018). The transcription factor-encoding gene crtf is involved in Clonostachys chloroleuca mycoparasitism on Sclerotinia sclerotiorum. Microbiological research, 210, 6-11.
58. Tapwal, A., Singh, U., Singh, G., Garg, S., & Kumar, R. (2011). In vitro antagonism of Trichoderma viride against five phytopathogens. Pest Technol, 5(1), 59-62. Townsend, G. R. (1943). Methods for estimating losses caused by diseases in fungicide experiments. Plant Disease Reporter, 27, 340-343.
59. Turhan, M. H. A. G., & Turhan, G. (2009). Rhizoctonia solani'nin Fungal Antagonistlerinin Belirlenmesi Üzerinde Araştırmalar. Anadolu Ege Tarımsal Araştırma Enstitüsü Dergisi, 19(2), 49-72.
60. Varo, A., Raya‐Ortega, M. C., & Trapero, A. (2016). Selection and evaluation of micro‐organisms for biocontrol of Verticillium dahliae in olive. Journal of Applied Microbiology, 121(3), 767-777.
61. Veronese, P., Narasimhan, M. L., Stevenson, R. A., Zhu, J. K., Weller, S. C., Subbarao, K. V., & Bressan, R. A. (2003). Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. The Plant Journal, 35(5), 574-587.
62. Woo, S. L., Scala, F., Ruocco, M., & Lorito, M. (2006). The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology, 96(2), 181-185.
63. Yiğit, F. (1993). Domateslerde Erken Yanıklık Hastalıgına Karsı Biyolojik Savasta Verticillium psalliotae Treschow ‘nin Etkinligi Üzerinde Arastırmalar (Doctoral dissertation, Yüksek Lisans Tezi), Ege Üniversitesi, Bitki Koruma Anabilim Dalı, İZMİR.
64. Yohalem, D. S., Nielsen, K., Green, H., & Funck Jensen, D. (2004). Biocontrol agents efficiently inhibit sporulation of Botrytis aclada on necrotic leaf tips but spread to adjacent living tissue is not prevented. FEMS microbiology ecology, 47(3), 297-303.
65. Zeise, K., & Von Tiedemann, A. (2002). Host specialization among vegetative compatibility groups of Verticillium dahliae in relation to Verticillium longisporum. Journal of Phytopathology, 150(3), 112-119.