Trichoderma harzianum Rifai (Ascomycota: Hypocreales)’nin Biber Bitkisi Aracılı Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)’nin Biyolojik Özelliklerine Etkisi

Öz

Amaç: Faydalı mikroorganizmalardan Trichoderma harzianum’un bitki köklerine kolonize olması sonucunda bitkilerin bağışıklık sistemini uyararak herbivor böceklere karşı savunma sağladığı bildirilmiştir. Bu çalışmada, T. harzianum'un Demre tipi biber bitkileri üstünde Myzus persicae'nin biyolojik özellikleri üzerine etkileri kontrollü koşullar altında (25±2 °C sıcaklık, %65±5 bağıl nem ve 16:8 aydınlık: karanlık) araştırılmıştır. Materyal ve Yöntem: Köklerine Trichoderma harzianum’un kolonizasyonu sağlanan biber bitkileri üstünde beslenen Myzus persicae’den günlük sayımlarla elde edilen ham veriler yaşam tablosu analizine tabi tutulmuştur. Araştırma Bulguları: Analiz sonuçlarına göre, kalıtsal üreme yeteneği (r) kontrol grubunda 0,3148 d⁻¹ ve T. harzianum uygulamasında 0,3304 d⁻¹, artış oranı hızı (λ) ise sırasıyla 1,3701 d⁻¹ ve 1,3916 d⁻¹ olarak bulunmuştur. Net üreme gücü (R₀) kontrol grubunda 68,26 yavru/birey, T. harzianum uygulamasında ise 65,65 yavru/birey olarak belirlenmiştir. Kontrol (2,2 gün) ile T. harzianum uygulaması (2,1 gün) arasındaki popülasyonun ikiye katlanma süresi farkının istatistiksel olarak önemsiz olduğu bulunmuştur. Sonuç: Çalışmanın sonucunda, köklerine T. harzianum kolonize edilen Demre tipi sivri biber bitkileri üzerinde beslenen M. persicae'nin biyolojik özellikleri üzerinde herhangi bir etkisinin olmadığı belirlenmiştir.

Anahtar Kelimeler

• Yaş ve döneme özgü iki eşeyli yaşam tablosu
• biyolojik özellikler
• Myzus persicae
• biber bitkisi
• Trichoderma harzianum

Effect of Trichoderma harzianum Rifai (Ascomycota: Hypocreales) on the Biological Traits of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) Mediated by Pepper Plant

Abstract

Objective: It has been reported that the colonization of plant roots by the beneficial microorganism Trichoderma harzianum triggers the plant’s immune system, providing defense against herbivorous insects. In this study, the effects of T. harzianum on the biological traits of Myzus persicae on pepper plants were investigated under controlled conditions (25±2°C, 65±5 RH, and a 16:8 light: dark). Materials and Methods: The raw data obtained from daily counts of Myzus persicae feeding on pepper plants whose roots were colonized by Trichoderma harzianum were subjected to life table analysis. Results: According to the analysis results, the intrinsic rate of increase (r) was 0.3148 d⁻¹ in the control and 0.3304 d⁻¹ in the T. harzianum treatment, while the finite rate of increase (λ) was 1.3701 d⁻¹ and 1.3916 d⁻¹, respectively. The net reproductive rate (R₀) was determined as 68.26 offspring/individual in the control and 65.65 offspring/individual in the T. harzianum treatment. The difference in population doubling time between the control (2.2 days) and T. harzianum treatment (2.1 days) was found to be statistically insignificant. Conclusion: As a result of the study, it was determined that there was no effect of T. harzianum colonization on the biological traits of M. persicae feeding on Demre-type pepper plants.

Keywords

• Age-stage two-sex life table
• Biological traits
• Myzus persicae
• Pepper plant
• Trichoderma harzianum

References

1. Abdel-Fattah, G. M., Shabana, Y. M., Ismail, A. E., & Rashad, Y. M. (2007). Trichoderma harzianum: a biocontrol agent against Bipolaris oryzae. Mycopathologia, 164(2), 81-89. https://doi.org/10.1007/s11046-007-9032-9
2. Adeleke, B. S., & Babalola, O. O. (2022). Roles of plant endosphere microbes in agriculture-a review. Journal of Plant Growth Regulation, 41(4), 1411-1428. https://doi.org/10.1007/s00344-021-10406-2
3. Aktar, W., Sengupta, D., & Chowdhury, A. (2009). Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary toxicology, 2(1), 1-12. https://doi.org/10.2478/v10102-009-0001-7
4. Al-Hazmi, A. S., & TariqJaveed, M. (2016). Effects of different inoculum densities of Trichoderma harzianum and Trichoderma viride against Meloidogyne javanica on tomato. Saudi Journal of Biological Sciences, 23(2), 288-292. https://doi.org/10.1016/j.sjbs.2015.04.007
5. Alınç, T., Cusumano, A., Peri, E., Torta, L., & Colazza, S. (2021). Trichoderma harzianum strain T22 modulates direct defense of tomato plants in response to Nezara viridula feeding activity. Journal of chemical ecology, 47(4), 455-462. https://doi.org/10.1007/s10886-021-01260-3
6. Aranega-Bou, P., de la O Leyva, M., Finiti, I., García-Agustín, P., & González-Bosch, C. (2014). Priming of plant resistance by natural compounds. Hexanoic acid as a model. Frontiers in plant science, 5, 488. https://doi.org/10.3389/fpls.2014.00488
7. Balog, A., Loxdale, H. D., Bálint, J., Benedek, K., Szabó, K. A., Jánosi-Rancz, K. T., & Domokos, E. (2017). The arbuscular mycorrhizal fungus Rhizophagus irregularis affects arthropod colonization on sweet pepper in both the field and greenhouse. Journal of Pest Science, 90, 935-946. https://doi.org/10.1007/s10340-017-0844-1
8. Bardin, M., Ajouz, S., Comby, M., Lopez-Ferber, M., Graillot, B., Siegwart, M., & Nicot, P. C. (2015). Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides?. Frontiers in Plant Science, 6, 566. https://doi:10.3389/fpls.2015.00566

9. Battaglia, D., Mang, S. M., Caccavo, V., Fanti, P., & Forlano, P. (2024). The Belowground–Aboveground Interactions of Zucchini: The Effects of Trichoderma afroharzianum Strain T22 on the Population and Behavior of the Aphid Aphis gossypii Glover and Its Endoparasitoid Aphidius colemani Viereck. Insects, 15(9),690. https://doi.org/10.3390/insects15090690
10. Beck, J. J., Alborn, H. T., Block, A. K., Christensen, S. A., Hunter, C. T., Rering, C. C., ... & Tumlinson, J. H. (2018). Interactions among plants, insects, and microbes: elucidation of inter-organismal chemical communications in agricultural ecology. Journal Of Agricultural And Food Chemistry, 66(26), 6663-6674. http://dx.doi.org/10.1021/acs.jafc.8b01763
11. Biryol, S., Demirbağ, Z., Erdoğan, P., & Demir, I. (2022). Development of Beauveria bassiana (Ascomycota: Hypocreales) as a mycoinsecticide to control green peach aphid, Myzus persicae (Homoptera: Aphididae) and investigation of its biocontrol potential. Journal of Asia-Pacific Entomology, 25(1), 101878. https://doi.org/10.1016/j.aspen.2022.101878
12. Carey, J. R. (1993). Applied demography for biologists: with special emphasis on insects. Oxford university press.
13. Chartrand, G., Polimeni, A. D. & Zhang P. (2008). Mathematical Proofs: A Transition to Advanced Mathematics. Boston, MA: Pearson Education, Inc. p. 491.
14. Chaverri, P., Castlebury, L. A., Overton, B. E., & Samuels, G. J. (2003). Hypocrea/Trichoderma: species with conidiophore elongations and green conidia. Mycologia,95(6),1100-1140. https://doi.org/10.1080/15572536.2004.11833023
15. Chi, H. (1988). Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17(1), 26-34. https://doi.org/10.1093/ee/17.1.26
16. Chi, H. (1990). Timing of control based on the stage structure of pest populations: a simulation approach. Journal of Economic entomology, 83(4), 1143-1150. https://doi.org/10.1093/jee/83.4.1143
17. Chi, H. (2024a). TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/Ecology/ (Accessed date: 07.01.2024).
18. Chi, H. (2024b). TIMING-MSChart: Computer program for population projection based on age-stage, two-sex life table. http://140.120.197.173/Ecology/ (Accessed date: 05.01.2024).
19. Chi, H., & Liu, H. (1985). Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 24(2), 225-240.
20. Chi, H., & Su, H. Y. (2006). Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead)(Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer)(Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environmental entomology, 35(1), 10-21. https://doi.org/10.1603/0046-225X-35.1.10
21. Chi, H., Güncan, A., Kavousi, A., Gharakhani, G., Atlihan, R., Özgökçe, M. S., … Taghizadeh, R. (2022a). TWOSEXMSChart: The key tool for life table research and education. Entomologia Generalis, 42(6), 845-849. https://doi.org/10.1127/entomologia/2022/1851
22. Chi, H., Kara, H., Özgökçe, M. S., Atlihan, R., Güncan, A., & Rişvanlı, M. R. (2022b). Innovative application of set theory, Cartesian product, and multinomial theorem in demographic research. Entomologia Generalis, 42(6). 863-874. https://doi.org/10.1127/entomologia/2022/1653
23. Contreras-Cornejo, H. A., Macías-Rodríguez, L., del-Val, E., & Larsen, J. (2018). The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Applied Soil Ecology, 124, 45-53. https://doi.org/10.1016/j.apsoil.2017.10.004
24. Contreras-Cornejo, H. A., Schmoll, M., Esquivel-Ayala, B. A., González-Esquivel, C. E., Rocha-Ramírez, V., & Larsen, J. (2024). Mechanisms for plant growth promotion activated by Trichoderma in natural and managed terrestrial ecosystems. Microbiological research, 281, 127621. https://doi.org/10.1016/j.micres.2024.127621
25. Coppola, M., Diretto, G., Digilio, M. C., Woo, S. L., Giuliano, G., Molisso, D., ... & Rao, R. (2019). Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defense responses against aphids. Frontiers in physiology, 10, 745. https://doi.org/10.3389/fphys.2019.00745
26. Dilmen, H. (2025). Trichoderma and Funneliformis Interactions: Influencing the Life Cycle and Population Dynamics of Myzus persicae on Pepper. ACS Omega. https://doi.org/10.1021/acsomega.5c00545
27. Efron, B., & Tibshirani, R. J. (1993). An Introduction to the Bootstrap. Chapman & Hall/CRC Monographs on Statistics and Applied Probability, New York. p. 430.
28. FAO, (2025). Birleşmiş Milletler Gıda ve Tarım Örgütü. Dünya Biber Üretim İstatistikleri. (Accessed date: 01.01.2025). https://www.fao.org/faostat/en/#data/QCL
29. Goodman, D., (1982). Optimal life histories, optimal notation, and the value of reproductive value. The American Naturalist, 119 (6): 803-823.
30. Harman, G. E. (2006). Overview of mechanisms and uses of Trichoderma spp. Phytopathology, 96(2), 190-194. https://doi.org/10.1094/PHYTO-96-0190
31. Hermosa, R., Rubio, M. B., Cardoza, R. E., Nicolás, C., Monte, E., & Gutiérrez, S. (2013). The contribution of Trichoderma to balancing the costs of plant growth and defense. Int. Microbiol, 16(2), 69-80. https://doi.org/10.2436/20.1501.01.181
32. Kara, H. (2025). Effect of Trichoderma harzianum Rifai and Trichoderma viride Pers.(Ascomycota: Hypocreales) on demographic parameters of Myzus persicae (Sulzer, 1776)(Hemiptera: Aphididae) feeding on bell pepper plant. Turkish Journal of Entomology, 49(2), 175-185. https://doi.org/10.16970/entoted.1572732
33. Liang, Y. R., Liao, F. C., & Huang, T. P. (2022). Deciphering the influence of Bacillus subtilis strain Ydj3 colonization on the vitamin C contents and rhizosphere microbiomes of sweet peppers. Plos one, 17(2), 1-14. https://doi.org/10.1371/journal.pone.0264276
34. López-Bucio, J., Esparza-Reynoso, S., & Pelagio-Flores, R. (2022). Nitrogen availability determines plant growth promotion and the induction of root branching by the probiotic fungus Trichoderma atroviride in Arabidopsis seedlings. Archives of microbiology, 204(7), 380. https://doi.org/10.1007/s00203-022-03004-7
35. Macías-Rodríguez, L., Contreras-Cornejo, H. A., Adame-Garnica, S. G., Del-Val, E., & Larsen, J. (2020). The interactions of Trichoderma at multiple trophic levels: inter-kingdom communication. Microbiological Research, 240, 126552. https://doi.org/10.1016/j.micres.2020.126552
36. Mukherjee, A., & Ghosh, S. K. (2023). An eco-friendly approach of biocontrol of aphid (Aphis gossypii Glover) by Trichoderma harzianum. Environmental Monitoring and Assessment, 195(1), 102. https://doi.org/10.1007/s10661-022-10726-0
37. Noman, A., Aqeel, M., Qasim, M., Haider, I., & Lou, Y. (2020). Plant-insect-microbe interaction: A love triangle between enemies in ecosystem. Science of the Total Environment, 699, 134181. https://doi.org/10.1016/j.scitotenv.2019.134181
38. Özgökçe M.S., Kara, H., Khitilov S., Doğaç M., Çakmak, S., Koyunçi G. (2025a). Effects of Trichoderma harzianum and Chaetomium cupreum on demography of Myzus persicae via Kapia Pepper Plant. 76th International Symposium on Crop Protection (Abstract/Poster), Ghent, Belgium.
39. Özgökçe, M.S., Ağca, E., Kara, H., Doğaç M. (2025b). Population parameters of Myzus persicae in different pepper cultivars treated with Trichoderma viride. 76th International Symposium on Crop Protection (Abstract/Oral), Ghent, Belgium.
40. Pieterse, C. M. J., Christos, Z., Roeland, L. B., David M., W., Saskia C.M., V. W. ve Peter A.H.M., B. (2014). Induced Systemic Resistance by Beneficial Microbes. Annual Review of Phytopathology, 52(1), 347-375. https://doi.org/10.1146/annurev-phyto-082712-102340
41. Pineda, A., Soler, R., Pozo, M. J., Rasmann, S., & Turlings, T. C. (2015). Above-belowground interactions involving plants, microbes and insects. Frontiers in Plant Science, 6, 318. https://doi.org/10.1146/annurev-phyto-082712-102340
42. Pineda, A., Zheng, S. J., van Loon, J. J., Pieterse, C. M., & Dicke, M. (2010). Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in plant science, 15(9), 507-514. https://doi.org/10.1016/j.tplants.2010.05.007
43. Sharma, G., Malthankar, P. A., & Mathur, V. (2021). Insect–plant interactions: a multilayered relationship. Annals of the Entomological Society of America, 114(1), 1-16. https://doi.org/10.1093/aesa/saaa032
44. Trotta, V., Russo, D., Rivelli, A. R., Battaglia, D., Bufo, S. A., Caccavo, V., ... & Brienza, M. (2024). Wastewater irrigation and Trichoderma colonization in tomato plants: effects on plant traits, antioxidant activity, and performance of the insect pest Macrosiphum euphorbiae. Environmental Science and Pollution Research, 31(12), 18887-18899. https://doi.org/10.1007/s11356-024-32407-w
45. Verdugo, J. A., Méndez, T., Ortiz–Martínez, S. A., Cumsille, R., & Ramírez, C. C. (2012). Variation in resistance mechanisms to the green peach aphid among different Prunus persica commercial cultivars. Journal of economic entomology, 105(5), 1844-1855. https://doi.org/10.1603/EC12100
46. Verma, P. P., Shelake, R. M., Das, S., Sharma, P., & Kim, J. Y. (2019). Plant growth-promoting rhizobacteria (PGPR) and fungi (PGPF): potential biological control agents of diseases and pests. In Microbial Interventions in Agriculture and Environment: Volume 1: Research Trends, Priorities and Prospects (pp. 281-311). Singapore: Springer.
47. Wielkopolan, B. ve Obrępalska, A. (2016). Three-way interaction among plants, bacteria, and coleopteran insects. Planta, 244(2), 313-332. https://doi.org/10.1007/s00425-016-2543-1
48. Woo, S. L., Hermosa, R., Lorito, M., & Monte, E. (2023). Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nature Reviews Microbiology, 21(5), 312-326. https://doi.org/10.1038/s41579-022-00819-5