Potential Efficiency of Aspergillus chevalieri Against Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) Larvae: Conidial Suspension and Ethanol Extract

Öz

In recent years, there has been a notable increase in research data supporting the use of fungal species from diverse genera such as Penicillium, Aspergillus, Fusarium, Beauveria, Cordyceps, Metarhizium, and Purpureocillium in biological control applications. The current study was conducted to identify Aspergillus chevalieri using morphological characteristics and molecular data, then to determine the potential efficiency of conidial suspension and ethanol extract against Ephestia kuehniella and to investigate its mycotoxin production potential and cytotoxicity. The identification was carried out using phenotypic characteristics and sequences of the internal transcribed spacer (ITS), beta-tubulin gene (benA), and RNA polymerase II second largest subunit (RPB2) loci. In developmental biology studies, it was determined that topically applied conidial suspensions and ethanol extracts at varying concentrations affected different life stages of the insect. In the conidial suspension treatments, the larval period (at 10⁸ conidia/mL) and pupal period (at 10⁶, 10⁷, and 10⁸ conidia/mL) were notably shortened compared to the control group. In ethanol extract applications, the adult emergence time was reduced at the lowest concentrations (0.5 mg/mL and 1 mg/mL). Furthermore, both conidial suspensions and ethanol extracts caused a significant decrease in the total number of eggs, depending on the concentration applied. In the cytotoxicity test, the ethanol extract of the fungus was found to be cytotoxic in the L929 mouse cell line (NCTC clone 929) at concentrations above 0.78 mg/mL. This study showed that the fungus does not produce aflatoxin and ochratoxin and provided the first information on its potential efficiency against E. kuehniella larvae. Based on the present findings, A. chevalieri can be considered a promising candidate for inclusion in biological control programs. To fully assess its potential, future studies should explore its efficacy against a broader range of pest species and conduct field trials under diverse environmental conditions to validate the laboratory results.

Anahtar Kelimeler

• Fungal identification
• fungal pathogenicity
• developmental biology
• biological control
• sustainable agriculture

Aspergillus chevalieri'nin Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) Larvalarına Karşı Potansiyel Etkinliği: Konidial Süspansiyon ve Etanol Ekstraktı

Öz

Son yıllarda, Penicillium, Aspergillus, Fusarium, Beauveria, Cordyceps, Metarhizium ve Purpureocillium gibi çeşitli cinslere ait mantar türlerinin biyolojik mücadelede kullanılmasına yönelik araştırma verilerinde dikkate değer bir artış yaşanmıştır. Bu çalışma, Aspergillus chevalieri'nin morfolojik özellikleri ve moleküler veriler kullanılarak tanımlanması, ardından konidiyum süspansiyonu ve etanol ekstraktının Ephestia kuehniella'ya karşı potansiyel etkinliğinin belirlenmesi ve ayrıca mikotoksin üretim potansiyeli ile sitotoksisitesinin araştırılması amacıyla gerçekleştirilmiştir. Tanımlamada; fenotipik özelliklere ek olarak iç transkribe edilen aralık (ITS), beta-tübülin (benA) ve RNA polimeraz II'nin ikinci büyük alt birimi (RPB2) gen bölgelerinin dizileri kullanılmıştır. Gelişim biyolojisi çalışmalarında, topikal olarak uygulanan farklı dozlardaki konidiyal süspansiyonların ve etanol ekstraktlarının böceğin farklı gelişim evrelerinde etkili olduğu belirlendi. Konidiyal süspansiyon uygulamalarında özellikle kontrole göre larval periyodun (108 konidia/mL) ve pupal periyodun (106, 107, 108 konidia/mL) kısaldığı görülürken, etanol ekstresi uygulamalarında ise en düşük dozlarda ergin çıkış süresinin (0.5 mg/mL ve 1 mg/mL) kısaldığı görülmüştür. Ayrıca, hem konidial süspansiyonların hem de etanol ekstraktının konsantrasyonuna bağlı olarak kontrole göre yumurta sayısında önemli azalmalar görülmüştür. Sitotoksisite testinde ise fungusun etanol ekstraktı, 0.78 mg/mL üzerindeki konsantrasyonlarda L929 fare hücre hattı (NCTC clone 929) üzerinde sitotoksik etki göstermiştir. Çalışma ayrıca, bu mantarın aflatoksin ve okratoksin üretmediğini ortaya koymuş ve E. kuehniella larvalarına karşı potansiyel etkinliği konusunda ilk bilgileri sunmuştur. Elde edilen bulgulara dayanarak, A. chevalieri biyolojik mücadele programlarına dahil edilebilecek umut verici bir aday olarak değerlendirilebilir. Bu potansiyelin tam olarak anlaşılabilmesi için, gelecekte yapılacak araştırmalarda A. chevalieri’nin farklı zararlı türleri üzerindeki etkisinin değerlendirilmesi ve çeşitli çevresel koşullarda saha denemelerinin gerçekleştirilmesi gerekmektedir.

Anahtar Kelimeler

• Fungal tanılama
• fungal patojenite
• gelişim biyolojisi
• biyolojik kontrol
• sürdürülebilir tarım

Kaynakça

1. Alikhani, M., Safavi, S.A., & Iranipou, S. (2019). Effect of the entomopathogenic fungus, Metarhizium anisopliae (Metschnikoff) Sorokin, on demographic fitness of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Egyptian Journal of Biological Pest Control, 29, 1-7. https://doi.org/10.1186/s41938-019-0121
2. Bovio, E., Garzoli, L., Poli, A., Luganini, A., Villa, P., Musumeci, R., McCormack, G.P., Cocuzza, C.E., Gribaudo, G., Mehiri, M., & Varese, G.C. (2019). Marine fungi from the sponge Grantia compressa: biodiversity, chemodiversity, and biotechnological potential. Marine drugs, 17(4), 220. https://doi.org/10.3390/md17040220
3. Castillo, M.A., Moya, P., Hernández, E., & Primo-Yufera, E. (2000). Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biological control, 19(3), 274-282. https://doi.org/10.1006/bcon.2000.0867
4. Chandler, D. (2017). Basic and applied research on entomopathogenic fungi. In Microbial control of insect and mite pests (pp. 69-89). Academic Press.
5. Chen, W., Xie, W., Cai, W., Thaochan, N., & Hu, Q. (2021). Entomopathogenic Fungi Biodiversity in the Soil of Three Provinces Located in Southwest China and First Approach to Evaluate Their Biocontrol Potential. Journal of Fungi, 7, 984. https://doi.org/10.3390/jof7110984
6. Chevrette, M.G., Carlson, C.M., Ortega, H.E., Thomas, C., Ananiev, G.E., Barns, K.J., & Currie, C.R. (2019). The antimicrobial potential of Streptomyces from insect microbiomes. Nature Communications, 10(1), 516. https://doi.org/10.1038/s41467-019-08438-0
7. de Oliveira, G.P., Barreto, D.L.C., Ramalho Silva, M., Augusti, R., Evódio Marriel, I., Gomes de Paula Lana, U., & Takahashi, J.A. (2022). Biotic stress caused by in vitro co-inoculation enhances the expression of acetylcholinesterase inhibitors by fungi. Natural Product Research, 36(16), 4266-4270. https://doi.org/10.1080/14786419.2021.1975701
8. Deka, B., Baruah, C., & Babu, A. (2021). Entomopathogenic microorganisms: their role in insect pest management. Egyptian Journal of Biological Pest Control, 31, 1-8. https://doi.org/10.1186/s41938-021-00466-7

9. Diao, H., Xing, P., Tian, J., Han, Z., Wang, D., Xiang, H., ... & Ma, R. (2022). Toxicity of crude toxin protein produced by Cordyceps fumosorosea IF-1106 against Myzus persicae (Sulze). Journal of Invertebrate Pathology, 194, 107825. https://doi.org/10.1016/j.jip.2022.107825
10. Erzurum, K. (2001). Gıdalarda mikotoksin oluşumunu etkileyen faktörler. Gıda, 26 (4), 289-293. Retrieved from: https://dergipark.org.tr/tr/pub/gida/issue/6931/92553
11. Escriva, L., Agahi, F., Vila-Donat, P., Mañes, J., Meca, G., & Manyes, L. (2021). Bioaccessibility study of aflatoxin B1 and ochratoxin A in bread enriched with fermented milk whey and/or pumpkin. Toxins, 14(1), 6. https://doi.org/10.3390/toxins14010006
12. Fancelli, M., Dias, A.B., Delalibera, I.J., Cerqueira de Jesus, S., Souza do Nascimento, A., & Oliveira e Silva, S. (2013). Beauveria bassiana Strains for Biological Control of Cosmopolites sordidus (Germ.) (Coleoptera: Curculionidae) in Plantain. BioMed Research International, 2013(1), 184756. https://doi.org/10.1155/2013/184756
13. Fujita, S. (2013). Simple modified method for fungal slide preparation. Journal of Medical Mycology, 54(2), 141-146. https://doi.org/10.3314/mmj.54.141
14. Glass, N.L., & Donaldson, G.C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61(4), 1323-30. https://10.1128/aem.61.4.1323-1330, PMID: 7747954; PMCID: PMC167388.
15. Gökçe, A., & Er, M.K. (2003). First description of the disease by Conidiobolus osmodes on Tipula paludosa larvae with the report of a natural epizootic. Journal of Invertebrate Pathology, 84(2), 83-89. https://doi.org/10.1016/j.jip.2003.09.004
16. Gradmann, C. (2008). A matter of methods: the historicity of Koch's postulates. Medical Journal, 43(2), 121–148. https://www.jstor.org/stable/25805450
17. Güner, P., Aşkun, T., & Er, A. (2023). Entomopathogenic Fungi and Their Potential Role in the Sustainable Biological Control of Storage Pests. Commagene Journal of Biology, 7(1), 90-97. https://doi.org/10.31594/commagene.1284354
18. Güner, P., Aşkun, T., Er, A., & Sönmez, D.G. (2025). Assessment of the potential pathogenicity of Penicillium mallochii conidial suspensions and ethanol extract against almond moth Cadra cautella (Walker) (Lepidoptera: Pyralidae). Journal of Plant Diseases and Protection, 132, 3. https://doi.org/10.1007/s41348-024-01039-0
19. Guo ZhiKai, G.Z., Gai CuiJuan, G.C., Cai CaiHong, C.C., Chen LiangLiang, C.L., Liu ShouBai, L.S., Zeng YanBo, Z.Y., Mei, W., & Dai HaoFu, D.H. (2017). Metabolites with insecticidal activity from Aspergillus fumigatus JRJ111048 isolated from mangrove plant Acrostichum specioum endemic to Hainan Island. Marine Drugs, 15(12), 381. https://doi.org/10.3390/md15120381
20. Guyonnet, D., Belloir, C., Suschetet, M., Siess, M.H., & Le Bon, A.M. (2002). Mechanisms of Protection Against Aflatoxin B(1) Genotoxicity in Rats Treated by Organosulfur Compounds from Garlic. Carcinogenesis, 23(8), 1335-1341. https://doi.org/10.1093/carcin/23.8.1335
21. Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. In Nucleic Acids Symposium Series, 41, 95–98.
22. Imamura, T., Todoriki, S., Sota, N., & Nakakita, H. (2004). Efect of sof-electron (low-energy electron) treatment on three stored-product insect pests. Journal of Stored Products Research, 40(2), 169–177. https://doi.org/10.1016/S0022-474X(02)00095-4
23. Jacob, T.A., & Cox, P.D. (1977). The influence of temperature and humidity on the life-cycle of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Journal of Stored Products Research, 13(3), 107-118. https://doi.org/10.1016/0022-474X(77)90009-1
24. Karthi, S., Vaideki, K., Shivakumar, M.S., Ponsankar, A., Thanigaivel, A., Chellappandian, M., Hunter, W.B., & Senthil-Nathan, S. (2018). Effect of Aspergillus flavus on the mortality and activity of antioxidant enzymes of Spodoptera litura Fab. (Lepidoptera: Noctuidae) larvae. Pesticide Biochemistry and Physiology, 149, 54-60. https://doi.org/10.1016/j.pestbp.2018.05.009
25. Kaur, S., Thakur, A., & Rajput, M. (2014). A laboratory assessment of the potential of Beauveria bassiana (Balsamo) Vuillemin as a biocontrol agent of Corcyra cephalonica Stainton (Lepidoptera: Pyralidae). Journal of Stored Products Research, 59, 185–189. https://doi.org/10.1016/j.jspr.2014.08.004
26. Kaur, T., Kaur, J., Kaur, A., & Kaur, S. (2016). Larvicidal and growth inhibitory effects of endophytic Aspergillus niger on a polyphagous pest, Spodoptera litura. Phytoparasitica, 44, 465-476. https://doi.org/10.1007/s12600-016-0541-2
27. Khan, H.A.A., & Khan, T. (2023). Efficacy of entomopathogenic fungi against three major stored insect pests, Rhyzopertha dominica, Sitophilus zeamais and Trogoderma granarium. Journal of Stored Products Research, 104, 102188. https://doi.org/10.1016/j.jspr.2023.102188
28. Klich, M.A. (2002). Identification of common Aspergillus species. Centraalbureau voor schimmelcultures.
29. Koo, H.N., Yoon, S.H., Shin, Y.H., & Yoon, C. (2011). Efect of electron beam irradiation on developmental stages of Plutella xylostella (Lepidoptera: Plutellidae). Journal of Asia-Pacific Entomology, 14(3), 243–247. https://doi.org/10.1016/j.aspen.2011.03.001
30. Koo, H.N., Yun, S.H., Yoon, C., & Kim, G.H. (2012). Electron beam irradiation induces abnormal development and the stabilization of p53 protein of American serpentine leafminer, Liriomyza trifolii (Burgess). Radiation Physics and Chemistry, 81(1), 86–92. https://doi.org/10.1016/j.radphyschem.2011.09.008
31. Letunic, I., & Bork, P. (2024). Interactive Tree of Life (iTOL) v6: recent updates to the phylogenetic tree display and annotation tool. Nucleic Acids Research, 52(W1), W78-W82. https://doi.org/10.1093/nar/gkae268
32. Lin, W.J., Chiu, M.C., Lin, C.C., Chung, Y.K., & Chou, J.Y. (2021). Efficacy of Entomopathogenic fungus Aspergillus nomius against Dolichoderus thoracicus. BioControl, 66(4), 463-473. https://doi.org/10.1007/s10526-021-10086-7
33. Liu, S., Li, J., Feng, Q., Chu, L., Tan, Z., Ji, X., & Jin, P. (2023). Insecticidal Effect of the Entomopathogenic Fungus Lecanicillium araneicola HK-1 in Aphis craccivora (Hemiptera: Aphididae). Insects, 14(11), 860. https://doi.org/10.3390/insects14110860
34. Liu, Y.J., Whelen, S., & Hall, B.D. (1999). Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biology and Evolution, 16(12), 1799-1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
35. Los, A., & Strachecka, A. (2018). Fast and Cost-Effective Biochemical Spectrophotometric Analysis of Solution of Insect Blood and Body Surface Elution. Sensors, 18(5), 1494. https://doi.org/10.3390/s18051494
36. Mannaa, M., & Kim, K.D. (2017). Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology, 45(4), 240-254. https://doi.org/10.5941/MYCO.2017.45.4.240
37. Marcinkevicius, K., Salvatore, S.A., Bardon, A.D.V., Cartagena, E., Arena, M.E., & Vera, N.R. (2017). Insecticidal activities of diketopiperazines of Nomuraea rileyi entomopathogenic fungus. International Journal of Environment, Agriculture and Biotechnology, 2(4), 1586-1596. https://doi.org/10.22161/ijeab/2.4.18
38. Mensah, R.K., & Young, A. (2017). Microbial control of cotton pests: use of the naturally occurring entomopathogenic fungus Aspergillus sp.(BC 639) in the management of Bemisia tabaci (Genn.)(Hemiptera: Aleyrodidae) and beneficial insects on transgenic cotton crops. Biocontrol Science and Technology, 27(7), 844-866. https://doi.org/10.1080/09583157.2017.1349875
39. Mohanty, S.S., & Prakash, S. (2010). Comparative efficacy and pathogenicity of keratinophilic soil fungi against Culex quinquefasciatus larvae. Indian Journal of Microbiology, 50, 299-302. https://doi.org/10.1007/s12088-010-0051-8
40. Nguyen, B.T., Shuval, K., Bertmann, F., & Yaroch, A.L. (2015). The Supplemental Nutrition Assistance Program, food insecurity, dietary quality, and obesity among US adults. American Journal of Public Health, 105(7), 1453-1459. https://doi.org/10.2105/AJPH.2015.302580
41. Nguyen, H.C., Lin, K.H., Nguyen, T.P., Le, H. S., Ngo, K.N., Pham, D.C., Su, C.H., & Barrow, C.J. (2023). Isolation and Cultivation of Penicillium citrinum for Biological Control of Spodoptera litura and Plutella xylostella. Fermentation, 9(5), 438. https://doi.org/10.3390/fermentation9050438
42. Ningsih, B.N.S., Rukachaisirikul, V., Phongpaichit, S., Preedanon, S., Sakayaroj, J., & Muanprasat, C. (2023). A nonadride derivative from the marine-derived fungus Aspergillus chevalieri PSU-AMF79. Natural Product Research, 37(14), 2311-2318. https://doi.org/10.1080/14786419.2022.2039651
43. Orozco, R.A., Lee, M.M., & Stock, S.P. (2014). Soil sampling and isolation of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae). Journal of Visualized Experiments, 89, 52083. https://doi.org/10.3791/52083
44. Pitt, J.I. (2000). Toxigenic fungi and mycotoxins. British Medical Bulletin, 56(1), 184-192. https://doi.org/10.1258/0007142001902888
45. Roy, H., Steinkraus, D.C., Eilinberg, J., Hajek, A.E., & Pell, J.K. (2006). Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology, 51, 331–357. https://doi.org/10.1146/annurev.ento.51.110104.150941
46. Rumbos, C.I., & Athanassiou, C.G. (2017). Use of entomopathogenic fungi for the control of stored-product insects: can fungi protect durable commodities. Journal of Pest Science, 90, 839–854. https://doi.org/10.1007/s10340-017-0849-9
47. Şahin Taylan, Z., & Er, M.K. (2024). Mortality Effects of Beauveria bassiana and Purpureocillium lilacinum Isolates and Efficacy of a Wettable Formulation on Palemona prasina (Hemiptera: Pentatomidae) Nymphs. Kahramanmaraş Sütçü İmam Üniversitesi Tarım ve Doğa Dergisi, 27(6), 1392-1400. https://doi.org/10.18016/ksutarimdoga.vi.1425131
48. Sani, I., Ismail, S. I., Abdullah, S., Jalinas, J., Jamian, S., & Saad, N. (2020). A review of the biology and control of whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), with special reference to biological control using entomopathogenic fungi. Insects, 11(9), 619. https://doi.org/10.3390/insects11090619
49. Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., & White, M.M. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences, 109(16), 6241-6246. https://doi.org/10.1073/pnas.1117018109
50. Senthilkumar, N., Murugesan, S., & Babu, D.S. (2014). Metabolite profiling of the extracts of endophytic fungi of entomopathogenic significance, Aspergillus flavus and Nigrospora sphaerica isolated from tropical tree species of India, Tectona grandis L. Journal of Agriculture and Life Sciences, 1(1), 108-114.
51. Shahrajabian, M.H., Kuang, Y., Cui, H., Fu, L., & Sun, W. (2023). Metabolic changes of active components of important medicinal plants on the basis of traditional Chinese medicine under different environmental stresses. Current Organic Chemistry, 27(9), 782-806. https://doi.org/10.2174/1385272827666230807150910
52. Shakarami, J., Eftekharifar, R., Latifian, M., & Jafari, S. (2015). Insecticidal activity and synergistic effect of Beauvaria bassiana (Bals.) Vuill. and three botanical compounds against third instar larvae of Ephestia kuehniella Zeller. Research on Crops, 16(2), 296-303. https://doi.org/10.5958/2348-7542.2015.00044.3
53. Singh, B.K., Delgado-Baquerizo, M., Egidi, E., Guirado, E., Leach, J.E., Liu, H., & Trivedi, P. (2023). Climate change impacts on plant pathogens, food security and paths forward. Nature Reviews Microbiology, 21(10), 640-656. https://doi.org/10.1038/s41579-023-00900-7
54. Song, Y., Liu, X., Feng, S., Zhao, K., Qi, Z., Wu, W., ... & Qin, B. (2023). Discovery, Identification, and Insecticidal Activity of an Aspergillus flavus Strain Isolated from a Saline–Alkali Soil Sample. Microorganisms, 11(11), 2788. https://doi.org/10.3390/microorganisms11112788
55. Spescha, A., Weibel, J., Wyser, L., Brunner, M., Hermida, M.H., Moix, A., & Maurhofer, M. (2023). Combining entomopathogenic Pseudomonas bacteria, nematodes and fungi for biological control of a below-ground insect pest. Agriculture, Ecosystems & Environment, 348, 108414. https://doi.org/10.1016/j.agee.2023.108414
56. Srivastava, C.N., Maurya, P., Sharma, P., & Mohan, L. (2009). Prospective role of insecticides of fungal origin. Entomological Research, 39(6), 341-355. https://doi.org/10.1111/j.1748-5967.2009.00244.x
57. Talavera, G., & Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic biology, 56(4), 564-577. https://doi.org/10.1080/10635150701472164
58. Todoriki, S., Mahbub Hasan, M.D., Miyanoshita, A., & Imamura, T. (2006). Assessment of electron beam-induced DNA damage in larvae of chestnut weevil, Curculio sikkimensis (Heller) (Coleoptera: Curculionidae) using comet assay. Radiation Physics and Chemistry, 75(2), 292–296. https://doi.org/10.1016/j.radphyschem.2005.08.001
59. Wang, Z., Jin, Q., Li, Q., Ou, X., Li, S., Liu, Z., & Huang, J.A. (2022). Multiplex PCR identification of Aspergillus cristatus and Aspergillus chevalieri in Liupao tea based on orphan genes. Foods, 11(15), 2217. https://doi.org/10.3390/foods11152217
60. Warcup, J.H. (1955). On the origin of colonies of fungi developing on soil dilution plates. Transactions of the British Mycological Society, 38(3), 298-301. https://doi.org/10.1016/S0007-1536(55)80075-7
61. White, T.J., Bruns, T., Lee, S., & Taylor, J.W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds.) PCR Proto-cols: A Guide to Methods and Applications. Academic Press, Inc., New York, 315–322.
62. Yan, J., Liu, H., Idrees, A., Chen, F., Lu, H., Ouyang, G., & Meng, X. (2022). First record of Aspergillus fijiensis as an entomopathogenic fungus against Asian Citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae). Journal of Fungi, 8(11), 1222. https://doi.org/10.3390/jof8111222
63. Yun, S.H., Lee, S.W., Koo, H.N., & Kim, G.H. (2014). Assessment of electron beam-induced abnormal development and DNA damage in Spodoptera litura (F.) (Lepidoptera: Noctuidae). Radiation Physics and Chemistry, 96, 44–49. https://doi.org/10.1016/j.radphyschem.2013.08.008
64. Zhang, S., Huang, Z., Xu, H., Liu, Q., Jiang, Z., Yin, C., Han, G., Zhang, W., & Zhang, Y. (2024a). Biological control of wheat powdery mildew disease by the termite‐associated fungus Aspergillus chevalieri BYST01 and potential role of secondary metabolites. Pest Management Science, 80(4), 2011-2020. https://doi.org/10.1002/ps.7938
65. Zhang, P.Z.P., You YinWei, Y.Y., Song Yuan, S.Y., Wang YouZhi, W.Y., & Zhang Long, Z.L. (2015). First record of Aspergillus oryzae (Eurotiales: Trichocomaceae) as an entomopathogenic fungus of the locust, Locusta migratoria (Orthoptera: Acrididae). Biocontrol Science and Technolgy, 25, 1285–1298. https://doi.org/10.1080/09583157.2015.1049977
66. Zhang, Z., Tian, Y., Sui, L., Lu, Y., Cheng, K., Zhao, Y., Li, Q., & Shi, W. (2024b). First record of Aspergillus nomiae as a broad-spectrum entomopathogenic fungus that provides resistance against phytopathogens and insect pests by colonization of plants. Frontiers in Microbiology, 14, 1284276. https://doi.org/10.3389/fmicb.2023.1284276
67. Zin, W.W.M., Buttachon, S., Dethoup, T., Pereira, J.A., Gales, L., Inácio, Â., Costa, P.M., Lee, M., Şekeroğlu, N., Pinto, M.M.M., & Kijjoa, A. (2017). Antibacterial and antibiofilm activities of the metabolites isolated from the culture of the mangrove-derived endophytic fungus Eurotium chevalieri KUFA 0006. Phytochemistry, 141, 86-97. https://doi.org/10.1016/j.phytochem.2017.05.015