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Expression profiling of Spodoptera exigua (Lepidoptera: Noctuidae) microRNAs and microRNA core genes by Bacillus thuringiensis GS57 infection

Published online by Cambridge University Press:  16 September 2024

Bo Gao
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Yu-Jie Ji
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Dan Zhao
Affiliation:
College of Plant Protection, Hebei Agricultural University, Baoding 071001, China
Lu Zhang
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Han Wu
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Yi-Fan Xie
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Qiu-Yu Shi
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Wei Guo*
Affiliation:
Graduate School of Chinese Academy of Agricultural Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China College of Plant Protection, Hebei Agricultural University, Baoding 071001, China
*
Corresponding author: Wei Guo; Email: [email protected]

Abstract

MicroRNAs (miRNAs) are endogenous, non-coding RNAs, which are functional in a variety of biological processes through post-transcriptional regulation of gene expression. However, the role of miRNAs in the interaction between Bacillus thuringiensis and insects remains unclear. In this study, small RNA libraries were constructed for B. thuringiensis-infected (Bt) and uninfected (CK) Spodoptera exigua larvae (treated with double-distilled water) using Illumina sequencing. Utilising the miRDeep2 and Randfold, a total of 233 known and 726 novel miRNAs were identified, among which 16 up-regulated and 34 down-regulated differentially expressed (DE) miRNAs were identified compared to the CK. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that potential target genes of DE miRNAs were associated with ABC transporters, fatty acid metabolism and MAPK signalling pathway which are related to the development, reproduction and immunity. Moreover, two miRNA core genes, SeDicer1 and SeAgo1 were identified. The phylogenetic tree showed that lepidopteran Dicer1 clustered into one branch, with SeDicer1 in the position closest to Spodoptera litura Dicer1. A similar phylogenetic relationship was observed in the Ago1 protein. Expression of SeDicer1 increased at 72 h post infection (hpi) with B. thuringiensis; however, expression of SeDicer1 and SeAgo1 decreased at 96 hpi. The RNAi results showed that the knockdown of SeDicer1 directly caused the down-regulation of miRNAs and promoted the mortality of S. exigua infected by B. thuringiensis GS57. In conclusion, our study is crucial to understand the relationship between miRNAs and various biological processes caused by B. thuringiensis infection, and develop an integrated pest management strategy for S. exigua via miRNAs.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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Footnotes

*

These authors have contributed equally to this work.

References

Ambros, V, Bartel, B, Bartel, DP, Burge, CB, Carrington, JC, Chen, X, Dreyfuss, G, Eddy, SR, Griffiths-Jones, S, Marshall, M, Matzke, M, Ruvkun, G and Tuschl, T (2003) A uniform system for microRNA annotation. RNA 9, 277279.CrossRefGoogle ScholarPubMed
Baradaran, E, Moharramipour, S, Asgari, S and Mehrabadi, M (2019) Upregulation of Helicoverpa armigera core RNA interference genes by bacterial infections and its effect on the insect-bacteria interaction. Insect Molecular Biochemistry 28, 290299.CrossRefGoogle ScholarPubMed
Bel, Y, Ferré, J and Hernández-Martínez, P (2020) Bacillus thuringiensis toxins: functional characterization and mechanism of action. Toxins 12, 785.CrossRefGoogle ScholarPubMed
Bidari, F, Fathipour, Y, Asgari, S and Mehrabadi, M (2022) Targeting the microRNA pathway core genes, Dicer 1 and Argonaute 1, negatively affects the survival and fecundity of Bemisia tabaci. Pest Management Science 78, 42344239.CrossRefGoogle ScholarPubMed
Cai, Y, Yu, X, Hu, SM and Yu, J (2009) A brief review on the mechanisms of miRNA regulation. Genomics – Proteomics & Bioinformatics 7, 147154.CrossRefGoogle ScholarPubMed
Cheng, Y, Lu, TF, Guo, JL, Lin, Z, Jin, Q, Zhang, XM and Zou, Z (2022) Helicoverpa armigera miR-2055 regulates lipid metabolism via fatty acid synthase expression. Open Biology 12, 210307.CrossRefGoogle ScholarPubMed
Chen, D, Yang, X, Yang, D, Liu, Y, Wang, Y, Luo, X, Tang, L, Yi, M, Huang, Y, Liu, Y and Liu, Z (2023) The RNase III enzyme Dicer1 is essential for larval development in Bombyx mori. Insect Science 30, 13091324.CrossRefGoogle ScholarPubMed
Clément, T, Salone, V and Rederstorff, M (2015) Dual Luciferase Gene Reporter Assays to Study miRNA Function. New York: Humana Press.CrossRefGoogle ScholarPubMed
Crickmore, N, Berry, C, Panneerselvam, S, Mishra, R, Connor, TR and Bonning, BC (2021) A structure-based nomenclature for Bacillus thuringiensis and other bacteria-derived pesticidal proteins. Journal of Invertebrate Pathology 186, 107438.CrossRefGoogle ScholarPubMed
Cui, CL, Wang, Y, Li, YF, Sun, PL, Jiang, JY, Zhou, HN, Liu, JN and Wang, SB (2022) Expression of mosquito miRNAs in entomopathogenic fungus induces pathogen-mediated host RNA interference and increases fungal efficacy. Cell Reports 41, 111527.CrossRefGoogle ScholarPubMed
Denli, AM, Tops, BBJ, Plasterk, RHA, Ketting, RF and Hannon, GJ (2004) Processing of primary microRNAs by the Microprocessor complex. Nature 432, 231235.CrossRefGoogle ScholarPubMed
Fang, Z and Rajewsky, N (2011) The impact of miRNA target sites in coding sequences and in 3’ UTRs. PLoS ONE 6, e18067.CrossRefGoogle ScholarPubMed
Feng, HQ, Wu, KM, Cheng, DF and Guo, YY (2003) Radar observations of the autumn migration of the beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) and other moths in northern China. Bulletin of Entomological Research 93, 115124.CrossRefGoogle ScholarPubMed
Filipowicz, W, Bhattacharyya, SN and Sonenberg, N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nature Reviews Genetics 9, 102114.CrossRefGoogle ScholarPubMed
Greenberg, SM, Sappington, TW, Legaspi, BC, Liu, TX and Sétamou, M (2001) Feeding and life history of Spodoptera exigua (Lepidoptera: Noctuidae) on different host plants. Annals of the Entomology Society of America 94, 566575.CrossRefGoogle Scholar
Grizanova, EV, Dubovskiy, IM, Whitten, MMA and Glupov, VV (2014) Contributions of cellular and humoral immunity of Galleria mellonella larvae in defence against oral infection by Bacillus thuringiensis. Journal of Invertebrate Pathology 119, 4046.CrossRefGoogle ScholarPubMed
Grove, M, Kimble, W and McCarthy, WJ (2001) Effects of individual Bacillus thuringiensis insecticidal crystal proteins on adult Heliothis virescens (F.) and Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). BioControl 46, 321335.CrossRefGoogle Scholar
Hafeez, M, Ullah, F, Khan, MM, Li, X, Zhang, Z, Shah, S, Imran, M, Assiri, MA, Fernández-Grandon, GM, Desneux, N, Rehman, M, Fahad, S and Lu, Y (2022) Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review. Environmental Science and Pollution Research 29, 17461762.CrossRefGoogle ScholarPubMed
Han, F, Lu, A, Yuan, Y, Huang, W, Beerntsen, BT, Huang, J and Ling, E (2017) Characterization of an entomopathogenic fungi target integument protein, Bombyx mori single domain von Willebrand factor type C, in the silkworm, Bombyx mori. Insect Molecular Biochemistry 26, 308316.CrossRefGoogle ScholarPubMed
Hipfner, DR, Weigmann, K and Cohen, SM (2002) The bantam gene regulates Drosophila growth. Genetics 161, 15271537.CrossRefGoogle ScholarPubMed
Hussein, HM, Habuštová, O and Sehnal, F (2005) Beetle-specific Bacillus thuringiensis Cry3Aa toxin reduces larval growth and curbs reproduction in Spodoptera littoralis (Boisd.). Pest Management. Science 61, 11861192.CrossRefGoogle ScholarPubMed
Ji, YJ, Gao, B, Zhao, D, Wang, Y, Zhang, L, Wu, H, Xie, YF, Shi, QY and Guo, W (2024) Involvement of Sep38β in the insecticidal activity of Bacillus thuringiensis against beet armyworm, Spodoptera exigua (Lepidoptera). Journal of Agricultural and Food Chemistry 72, 23212333.CrossRefGoogle ScholarPubMed
Jin, Y, Chen, Z, Liu, X and Zhou, XF (2013) Evaluating the MicroRNA Targeting Sites by Luciferase Reporter Gene Assay. Totowa: Humana Press, pp. 117127.Google ScholarPubMed
Jouravleva, K, Golovenko, D, Demo, G, Dutcher, RC, Hall, TMT, Zamore, PD and Korostelev, AA (2022) Structural basis of microRNA biogenesis by Dicer-1 and its partner protein Loqs-PB. Molecular Cell 82, 40494063, e6.CrossRefGoogle ScholarPubMed
Krüger, J and Rehmsmeier, M (2006) RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Research 9, 277279.Google Scholar
Kubo, Y, Sekiya, S, Ohigashi, M, Takenaka, C, Tamura, K, Nada, S, Nishi, T, Yamamoto, A and Yamaguchi, A (2005) ABCA5 resides in lysosomes, and ABCA5 knockout mice develop lysosomal disease-like symptoms. Molecular and Cellular Biology 25, 41384149.CrossRefGoogle ScholarPubMed
Kuhn, DE, Martin, MM, Feldman, DS, Terry, AV, Nuovo, GJ and Elton, TS (2008) Experimental validation of miRNA targets. Methods 44, 4754.CrossRefGoogle ScholarPubMed
Lai, EC, Wiel, C and Rubin, GM (2004) Complementary miRNA pairs suggest a regulatory role for miRNA: miRNA duplexes. RNA 10, 171175.CrossRefGoogle ScholarPubMed
Lee, JY, Kim, S, Hwang, DW, Jeong, JM, Chung, JK, Lee, MC and Lee, DS (2008) Development of a dual-luciferase reporter system for in vivo visualization of MicroRNA biogenesis and posttranscriptional regulation. Journal of Nuclear Medicine 49, 285294.CrossRefGoogle ScholarPubMed
Lee, YY, Lee, H, Kim, H, Kim, VN and Roh, SH (2023) Structure of the human DICER–pre-miRNA complex in a dicing state. Nature 615, 331338.CrossRefGoogle Scholar
Lee, Y, Ahn, C, Han, J, Choi, H, Kim, J, Yim, J, Lee, J, Provost, P, Rådmark, O, Kim, S and Kim, VN (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415419.CrossRefGoogle ScholarPubMed
Li, S, Xu, X, Zheng, Z, Zheng, JL, Shakeel, M and Jin, FL (2019) MicroRNA expression profiling of Plutella xylostella after challenge with B. thuringiensis. Developmental and Comparative Immunology 93, 115124.CrossRefGoogle ScholarPubMed
Li, L, Zhu, B, Sun, X, Zheng, K, Liang, P and Gao, XW (2022a) miR-34-5p, a novel molecular target against lepidopteran pests. Journal of Pest Science 96, 209224.CrossRefGoogle Scholar
Li, YZ, Zhao, D, Wu, H, Ji, YJ, Liu, ZR, Guo, XC, Guo, W and Bi, Y (2022b) B. thuringiensis GS57 interaction with gut microbiota accelerates Spodoptera exigua mortality. Frontiers in Microbiology 13, 649.Google ScholarPubMed
Ling, L, Kokoza, VA, Zhang, CY, Aksoy, E and Raikhel, AS (2017) MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences 114, E8017E8024.CrossRefGoogle ScholarPubMed
Liu, ZC, Zhang, JB, Fang, B, Wu, QS and Weng, QB (2022) Cloning and expression stability analysis of Spodoptera exigua U6 snRNA. Jiangsu Agricultural Science 50, 5358.Google Scholar
Liu, L, Zhang, P, Gao, Q, Feng, XG, Han, L, Zhang, FB, Bai, YM, Han, MJ, Hu, H, Dai, FY, Zhang, GJ and Tong, XL (2021) Comparative transcriptome analysis reveals bmo-miR-6497-3p regulate circadian clock genes during the embryonic diapause induction process in bivoltine silkworm. Insects 12, 739.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.CrossRefGoogle Scholar
Llave, C, Xie, Z, Kasschau, KD and Carrington, JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 20532056.CrossRefGoogle ScholarPubMed
Love, MI, Huber, W and Anders, S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15, 121.CrossRefGoogle ScholarPubMed
Lucas, KJ, Zhao, B, Liu, S and Raikhel, AS (2015) Regulation of physiological processes by microRNAs in insects. Current Opinion in Insect Science 11, 17.CrossRefGoogle ScholarPubMed
Ma, L, Liu, L, Zhao, Y, Yang, L, Chen, CH, Li, ZF and Lu, ZQ (2020) JNK pathway plays a key role in the immune system of the pea aphid and is regulated by microRNA-184. PLoS Pathogens 16, e1008627.CrossRefGoogle Scholar
Maharjan, R, Ahn, J and Yi, H (2022) Interactive effects of temperature and plant host on the development parameters of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Insects 13, 747.CrossRefGoogle ScholarPubMed
Melo, ALA, Soccol, VT and Soccol, CR (2016) Bacillus thuringiensis: mechanism of action, resistance, and new applications: a review. Critical Reviews in Biotechnology 36, 317326.CrossRefGoogle ScholarPubMed
Mezzetti, B, Smagghe, G, Arpaia, S, Christiaens, O, Dietz-Pfeilstetter, A, Jones, H, Kostov, K, Sabbadini, S, Opsahl-Sorteberg, HG, Ventura, V, Taning, CNT and Sweet, J, (2020) RNAi: what is its position in agriculture? Journal of Pest Science 93, 11251130.CrossRefGoogle Scholar
Moulton, JK, Pepper, DA and Dennehy, TJ (2000) Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Managment Science 56, 842848.3.0.CO;2-H>CrossRefGoogle Scholar
Park, Y and Kim, Y (2013) RNA interference of cadherin gene expression in Spodoptera exigua reveals its significance as a specific Bt target. Journal of Invertebrate Pathology 114, 285291.CrossRefGoogle ScholarPubMed
Petriv, OI, Pilgrim, DB, Rachubinski, RA and Titorenko, VI (2002) RNA interference of peroxisome-related genes in C. elegans: a new model for human peroxisomal disorders. Physiological Genomics 10, 7991.CrossRefGoogle Scholar
Pfaffl, MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45e45.CrossRefGoogle ScholarPubMed
Price, DRG and Gatehouse, JA (2008) RNAi-mediated crop protection against insects. Trends in Biotechnology 26, 393400.CrossRefGoogle ScholarPubMed
Rabelo, MM, Santos, IB and Paula-Moraes, SV (2022) Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae) fitness and resistance stability to diamide and pyrethroid insecticides in the United States. Insects 13, 365.CrossRefGoogle ScholarPubMed
Rahimpour, H, Moharramipour, S, Asgari, S and Mehrabadi, M (2019) The microRNA pathway core genes are differentially expressed during the development of Helicoverpa armigera and contribute in the insect's development. Insect Biochemistry and Molecular Biology 110, 121127.CrossRefGoogle ScholarPubMed
Ren, XL, Chen, RR, Zhang, Y, Ma, Y, Cui, JJ, Han, ZJ, Mu, LL and Li, GQ (2013) A Spodoptera exigua cadherin serves as a putative receptor for Bacillus thuringiensis Cry1Ca toxin and shows differential enhancement of Cry1Ca and Cry1Ac toxicity. Applied and Environmental Microbiology 79, 55765583.CrossRefGoogle ScholarPubMed
Rodríguez-González, Á, Porteous-Álvarez, AJ, Del Val, M, Casquero, PA and Escriche, B (2020) Toxicity of five Cry proteins against the insect pest Acanthoscelides obtectus (Coleoptera: Chrisomelidae: Bruchinae). Journal of Invertebrate Pathology 169, 107295.CrossRefGoogle ScholarPubMed
Sanahuja, G, Banakar, R, Twyman, RM, Capell, T and Christou, P (2011) Bacillus thuringiensis: a century of research, development and commercial applications. Plant Biotechnology Journal 9, 283300.CrossRefGoogle ScholarPubMed
Simon, S, Breeschoten, T, Jansen, HJ, Dirks, RP, Schranz, ME and Ros, VID (2021) Genome and transcriptome analysis of the beet armyworm Spodoptera exigua reveals targets for pest control. G3–Genes Genomes Genetics 11, jkab311.CrossRefGoogle ScholarPubMed
Su, XD, Zhang, W, Yuan, YW, Li, YJ, Ma, W and Tan, JY (2007) Research on the diversity of Bacillus Thuringiensis in some areas of Hebei province. Journal of Anhui Agricultural Sciences 18, 55405541.Google Scholar
Tabashnik, BE, Carrière, Y, Dennehy, TJ, Morin, S, Sisterson, MS, Roush, RT, Shelton, AM and Zhao, JZ (2003) Insect resistance to transgenic Bt crops: lessons from the laboratory and field. Journal of Economic Entomology 96, 10311038.CrossRefGoogle ScholarPubMed
Tabashnik, BE, Van Rensburg, JBJ and Carrière, Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. Journal of Economic Entomology 102, 20112025.CrossRefGoogle ScholarPubMed
Tabashnik, BE, Liesner, LR, Ellsworth, PC, Unnithan, GC, Fabrick, JA, Naranjo, SE, Li, XC, Dennehy, TJ, Antilla, L, Staten, RT and Carrière, Y (2021) Transgenic cotton and sterile insect releases synergize eradication of pink bollworm a century after it invaded the United States. Proceedings of the National Academy of Sciences 118, e2019115118.CrossRefGoogle ScholarPubMed
Theodoulou, FL, Holdsworth, M and Baker, A (2006) Peroxisomal ABC transporters. Febs Letters 580, 11391155.CrossRefGoogle ScholarPubMed
Tian, LX, Song, TX, He, RJ, Zeng, Y, Xie, W, Wu, QJ, Wang, SL, Zhou, XG and Zhang, YJ (2017) Genome-wide analysis of ATP-binding cassette (ABC) transporters in the sweet potato whitefly, Bemisia tabaci. BMC Genomics 18, 116.CrossRefGoogle Scholar
Vaucheret, H, Vazquez, F, Crété, P and Bartel, DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Gene & Development 18, 11871197.CrossRefGoogle ScholarPubMed
Wang, XL, Lu, ZY, Li, JC, Li, Z, Dong, J and Liu, XX (2018) Effects of Cry1Ac and Cry2Ab protein on development of oriental armyworm, Mythimna separata (Walker) (Lepidoptera: Noctuidae). Chinese Journal of Applied Entomology 55, 875881.Google Scholar
Wei, X, Zheng, C, Peng, TF, Pan, YO, Xi, JH, Chen, XW, Zhang, JH, Yang, S, Gao, XW and Shang, QL (2016) miR-276 and miR-3016-modulated expression of acetyl-CoA carboxylase accounts for spirotetramat resistance in Aphis gossypii Glover. Insect Biochemistry and Molecular Biology 79, 5765.CrossRefGoogle Scholar
Xiong, Y, Zeng, H, Zhang, Y, Xu, D and Qiu, D (2013) Silencing the HaHR3 gene by transgenic plant-mediated RNAi to disrupt Helicoverpa armigera development. International Journal of Biological Sciences 9, 370381.CrossRefGoogle ScholarPubMed
Yang, ML, Wei, YY, Jiang, F, Wang, Y, Guo, XJ, He, J and Kang, L (2014) MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. PLoS Genetics 10, e1004206.CrossRefGoogle ScholarPubMed
Yang, J, Xu, X, Lin, S, Chen, SY, Lin, GF, Song, QS, Bai, JL, You, MS and Xie, M (2021) Profiling of microRNAs in midguts of Plutella xylostella provides novel insights into the Bacillus thuringiensis resistance. Frontiers in Genetics 12, 739849.CrossRefGoogle ScholarPubMed
Yu, HC, Wang, Y, Sun, LF, Zhang, BL, Li, SY, Zhang, MH and Hou, YM (2021) Effects of Bacillus thuringiensis on pathogenicity and growing development of Mythimna separata (Walker). Journal of Northeast Agricultural University 52, 2128.Google Scholar
Zeng, Q, Long, G, Yang, H, Zhou, C, Yang, X, Wang, Z and Jin, D (2023) SfDicer1 participates in the regulation of molting development and reproduction in the white-backed planthopper, Sogatella furcifera. Pesticide Biochemistry and Physiology 191, 105347.CrossRefGoogle ScholarPubMed
Zhang, X, Lu, K and Zhou, Q (2013a) Dicer 1 is crucial for the oocyte maturation of telotrophic ovary in Nilaparvata lugens (STÁL) (Hemiptera: Geometroidea). Archives of Insect Biochemistry and Physiology 84, 194208.CrossRefGoogle Scholar
Zhang, Y, Ma, Y, Wan, PJ, Mu, LL and Li, GQ (2013b) Bacillus thuringiensis insecticidal crystal proteins affect lifespan and reproductive performance of Helicoverpa armigera and Spodoptera exigua adults. Journal of Economic Entomology 106, 614621.CrossRefGoogle ScholarPubMed
Zhang, YL, Huang, QX, Yin, GH, Lee, S, Jia, RZ, Liu, ZX, Yu, NT, Pennerman, KK, Chen, X and Guo, AP (2015) Identification of microRNAs by small RNA deep sequencing for synthetic microRNA mimics to control Spodoptera exigua. Gene 557, 215221.CrossRefGoogle ScholarPubMed
Zhu, B, Sun, X, Nie, XM, Liang, P and Gao, XW (2020) MicroRNA-998-3p contributes to Cry1Ac-resistance by targeting ABCC2 in lepidopteran insects. Insect Biochemistry and Molecular Biology 117, 103283.CrossRefGoogle ScholarPubMed
Zuo, YY, Wang, ZY, Ren, X, Pei, YK, Aioub, AAA and Hu, ZN (2022) A Genetic compensation phenomenon and global gene expression changes in Sex-miR-2766-3p knockout strain of Spodoptera exigua Hübner (Lepidoptera: Noctuidae). Insects 13, 1075.CrossRefGoogle ScholarPubMed
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