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

Year 2025, Volume: 9 Issue: 2, 198 - 209

Pınar Güner , Tülin Aşkun , Aylin Er , Görkem Deniz Sönmez , Raziye Korkmaz

https://doi.org/10.31594/commagene.1709718

Abstract

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.

Keywords

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

Ethical Statement

Ethics committee approval is not required.

Supporting Institution

TÜBİTAK

Project Number

TUBITAK-1001 (122O398) and TUBITAK 2209-A Research Project Support Program for Undergraduate Students

Thanks

Our work was financially supported by TUBITAK-1001, The Scientific and Technological Research Projects Funding Program (122O398) and TUBITAK 2209-A Research Project Support Program for Undergraduate Students.

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

Abstract

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.

Keywords

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

Project Number

TUBITAK-1001 (122O398) and TUBITAK 2209-A Research Project Support Program for Undergraduate Students

References

• 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
• 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
• 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
• Chandler, D. (2017). Basic and applied research on entomopathogenic fungi. In Microbial control of insect and mite pests (pp. 69-89). Academic Press.
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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
• 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
• 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
• Klich, M.A. (2002). Identification of common Aspergillus species. Centraalbureau voor schimmelcultures.
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Pitt, J.I. (2000). Toxigenic fungi and mycotoxins. British Medical Bulletin, 56(1), 184-192. https://doi.org/10.1258/0007142001902888
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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.
• 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
• 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
• 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
• 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
• 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
• 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