Integrating Full-Length and Second-Generation Transcriptomes to Elucidate the ApNPV-Induced Transcriptional Reprogramming in Antheraea pernyi Midgut
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Preparation of Samples
2.2. PacBio Sequencing
2.3. Data Processing and Gene Model Optimization
2.4. Functional Annotation of Genes and Identification of lncRNAs
2.5. Identification of APA and AS Events
2.6. TF Identification and Analysis
2.7. Comparative Transcriptome Analysis of DEGs After ApNPV Infection
3. Results
3.1. PacBio Data Output
3.2. Determination of Novel Genes, LncRNAs, and TFs
3.3. Complex Regulation of RNA Transcription by AS and APA
3.4. Transcriptional Reprogramming in A. pernyi Midgut Following ApNPV Infection
3.5. Construction of the PPI Network of DEGs
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Liu, Y.; Li, Y.; Li, X.; Qin, L. The Origin and Dispersal of the Domesticated Chinese Oak Silkworm, Antheraea pernyi, in China: A Reconstruction Based on Ancient Texts. J. Insect Sci. 2010, 10, 180. [Google Scholar] [CrossRef]
- Lei, Y.; Li, Y.; Yang, X.; Zhu, X.; Zhang, X.; Du, J.; Liang, S.; Li, S.; Duan, J. A Gut-Specific LITAF- like Gene in Antheraea pernyi (Lepidoptera: Saturniidae) Involved in the Immune Response to Three Pathogens. J. Econ. Entomol. 2021, 114, 1975–1982. [Google Scholar] [CrossRef]
- Duan, J.; Liang, S.; Zhu, Z.; Yang, X.; Li, Y.; Xu, X.; Wang, J.; Zhu, X.; Yao, L. Tissue-Associated Profiling of Gene Expression in the Fifth-Instar Larvae of Chinese Oak Silkworm, Antheraea pernyi. J. Asia-Pac. Entomol. 2023, 26, 102093. [Google Scholar] [CrossRef]
- Wang, X.; Luo, H.; Zhang, R. Innate Immune Responses in the Chinese Oak Silkworm, Antheraea pernyi. Dev. Comp. Immunol. 2018, 83, 22–33. [Google Scholar] [CrossRef]
- Xia, J.; Peng, R.; Fei, S.; Awais, M.M.; Lai, W.; Huang, Y.; Wu, H.; Yu, Y.; Liang, L.; Swevers, L.; et al. Systematic Analysis of Innate Immune-related Genes in the Silkworm: Application to Antiviral Research. Insect Sci. 2025, 32, 151–171. [Google Scholar] [CrossRef]
- Tanaka, H.; Ishibashi, J.; Fujita, K.; Nakajima, Y.; Sagisaka, A.; Tomimoto, K.; Suzuki, N.; Yoshiyama, M.; Kaneko, Y.; Iwasaki, T. A Genome-Wide Analysis of Genes and Gene Families Involved in Innate Immunity of Bombyx mori. Insect Biochem. Mol. Biol. 2008, 38, 1087–1110. [Google Scholar] [CrossRef] [PubMed]
- Duan, X.; Fu, T.; Liu, C.; Wang, F.; Liu, C.; Zhao, L.; Yu, J.; Wang, X.; Zhang, R. The Role of a Novel Secretory Peptidoglycan Recognition Protein with Antibacterial Ability from the Chinese Oak Silkworm Antheraea pernyi in Humoral Immunity. Insect Biochem. Mol. Biol. 2024, 171, 104151. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Wang, Y.; Zhou, J.; Zhang, Y.; Ma, Y.; Wang, D.; Jiang, Y.; Shi, S.; Qin, L. Peptidoglycan Recognition Proteins Regulate Immune Response of Antheraea pernyi in Different Ways. J. Invertebr. Pathol. 2019, 166, 107204. [Google Scholar] [CrossRef]
- Kausar, S.; Abbas, M.N.; Qian, C.; Zhu, B.; Gao, J.; Sun, Y.; Wang, L.; Wei, G.; Liu, C. Role of Antheraea pernyi Serpin 12 in Prophenoloxidase Activation and Immune Responses. Arch. Insect Biochem. Physiol. 2018, 97, e21435. [Google Scholar] [CrossRef]
- Wang, L.; Yang, L.; Zhou, X.-S.; Li, T.-H.; Liu, C.-L. A Clip Domain Serine Protease Stimulates Melanization Activation and Expression of Antimicrobial Peptides in the Chinese Oak Silkworm, Antheraea pernyi. J. Asia-Pac. Entomol. 2018, 21, 864–871. [Google Scholar] [CrossRef]
- Kausar, S.; Abbas, M.N.; Qian, C.; Zhu, B.; Sun, Y.; Sun, Y.; Wang, L.; Wei, G.; Maqsood, I.; Liu, C.-L. Serpin-14 Negatively Regulates Prophenoloxidase Activation and Expression of Antimicrobial Peptides in Chinese Oak Silkworm Antheraea pernyi. Dev. Comp. Immunol. 2017, 76, 45–55. [Google Scholar] [CrossRef]
- Wang, X.; Wang, K.; He, Y.; Lu, X.; Wen, D.; Wu, C.; Zhang, J.; Zhang, R. The Functions of Serpin-3, a Negative-Regulator Involved in Prophenoloxidase Activation and Antimicrobial Peptides Expression of Chinese Oak Silkworm, Antheraea pernyi. Dev. Comp. Immunol. 2017, 69, 1–11. [Google Scholar] [CrossRef]
- Chen, Z.; Zhang, A.; Xu, X.; Ding, L.; Zhang, X.; Qian, C.; Zhu, B. Toll-Interacting Protein Participates in Immunity and Development of the Lepidopteran Insect Antheraea pernyi. Bull. Entomol. Res. 2023, 113, 497–507. [Google Scholar] [CrossRef]
- Sun, Y.; Jiang, Y.; Wang, Y.; Li, X.; Yang, R.; Yu, Z.; Qin, L. The Toll Signaling Pathway in the Chinese Oak Silkworm, Antheraea pernyi: Innate Immune Responses to Different Microorganisms. PLoS ONE 2016, 11, e0160200. [Google Scholar] [CrossRef] [PubMed]
- Satyavathi, V.V.; Mohamed, A.A.; Kumari, S.; Mamatha, D.M.; Duvic, B. The IMD Pathway Regulates Lysozyme-like Proteins (LLPs) in the Silkmoth Antheraea mylitta. J. Invertebr. Pathol. 2018, 154, 102–108. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L. Insights into the Antiviral Pathways of the Silkworm Bombyx mori. Front. Immunol. 2021, 12, 639092. [Google Scholar] [CrossRef] [PubMed]
- Crawford, L.V. Introduction: Virus–Host Interactions. Proc. R. Soc. Lond. B Biol. Sci. 1980, 210, 319–320. [Google Scholar] [CrossRef]
- Mothes, W.; Sherer, N.M.; Jin, J.; Zhong, P. Virus Cell-to-Cell Transmission. J. Virol. 2010, 84, 8360–8368. [Google Scholar] [CrossRef]
- Jiang, L.; Goldsmith, M.R.; Xia, Q. Advances in the Arms Race between Silkworm and Baculovirus. Front. Immunol. 2021, 12, 628151. [Google Scholar] [CrossRef]
- Zhao, S.; Wang, X.; Yang, T.; Zhu, X.; Wu, X. BmNPV Interacts with Super-Enhancer Regions of the Host Chromatin to Hijack Cellular Transcription Machinery. Nucleic Acids Res. 2025, 53, gkaf188. [Google Scholar] [CrossRef]
- Wang, G.; Na, S.; Duan, X.; Leng, Z.; Jiang, Y.; Shi, S.; Yang, R.; Qin, L. Transcriptome Sequencing to Unravel the Molecular Mechanisms Underlying the Cuticle Liquefaction of Antheraea pernyi Following Antheraea pernyi Nucleopolyhedrovirus Challenge. Mol. Immunol. 2019, 109, 108–115. [Google Scholar] [CrossRef]
- Liu, Y.; Xin, Z.-Z.; Song, J.; Zhu, X.-Y.; Liu, Q.-N.; Zhang, D.-Z.; Tang, B.-P.; Zhou, C.-L.; Dai, L.-S. Transcriptome Analysis Reveals Potential Antioxidant Defense Mechanisms in Antheraea pernyi in Response to Zinc Stress. J. Agric. Food Chem. 2018, 66, 8132–8141. [Google Scholar] [CrossRef]
- Xie, L.; Teng, K.; Tan, P.; Chao, Y.; Li, Y.; Guo, W.; Han, L. PacBio Single-Molecule Long-Read Sequencing Shed New Light on the Transcripts and Splice Isoforms of the Perennial Ryegrass. Mol. Genet. Genom. 2020, 295, 475–489. [Google Scholar] [CrossRef]
- Su, Z.; Huang, D. Alternative Splicing of Pre-mRNA in the Control of Immune Activity. Genes 2021, 12, 574. [Google Scholar] [CrossRef] [PubMed]
- He, Y.; Yang, X.; Xia, X.; Wang, Y.; Dong, Y.; Wu, L.; Jiang, P.; Zhang, X.; Jiang, C.; Ma, H.; et al. A Phase-Separated Protein Hub Modulates Resistance to Fusarium Head Blight in Wheat. Cell Host Microbe 2024, 32, 710–726.e10. [Google Scholar] [CrossRef]
- Kufel, J.; Diachenko, N.; Golisz, A. Alternative Splicing as a Key Player in the Fine-tuning of the Immunity Response in Arabidopsis. Mol. Plant Pathol. 2022, 23, 1226–1238. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Liu, W.; Guo, H.; Dang, Y.; Cheng, T.; Yang, W.; Sun, Q.; Wang, B.; Wang, Y.; Xie, E.; et al. Frontiers | Distinct Functions of Bombyx mori Peptidoglycan Recognition Protein 2 in Immune Responses to Bacteria and Viruses. Front. Immunol. 2019, 10, 776. [Google Scholar] [CrossRef]
- Xu, X.; Wang, K.; Zha, X. An Antisense lncRNA Functions in Alternative Splicing of Bmdsx in the Silkworm, Bombyx mori. Biochem. Biophys. Res. Commun. 2019, 516, 639–644. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Yin, H.; Shen, M.; Huang, H.; Hou, Q.; Zhang, Z.; Zhao, W.; Guo, X.; Wu, P. Analysis of lncRNA-Mediated Gene Regulatory Network of Bombyx mori in Response to BmNPV Infection. J. Invertebr. Pathol. 2020, 170, 107323. [Google Scholar] [CrossRef]
- Fan, Y.-X.; Andoh, V.; Chen, L. Multi-Omics Study and ncRNA Regulation of Anti-BmNPV in Silkworms, Bombyx mori: An Update. Front. Microbiol. 2023, 14, 1123448. [Google Scholar] [CrossRef]
- Zhang, Z.; Zhao, Z.; Lin, S.; Wu, W.; Tang, W.; Dong, Y.; Shen, M.; Wu, P.; Guo, X. Identification of Long Noncoding RNAs in Silkworm Larvae Infected with Bombyx mori Cypovirus. Arch. Insect Biochem. Physiol. 2021, 106, 1–12. [Google Scholar] [CrossRef]
- Duan, J.; Li, Y.; Du, J.; Duan, E.; Lei, Y.; Liang, S.; Zhang, X.; Zhao, X.; Kan, Y.; Yao, L.; et al. A Chromosome-scale Genome Assembly of Antheraea pernyi (Saturniidae, Lepidoptera). Mol. Ecol. Resour. 2020, 20, 1372–1383. [Google Scholar] [CrossRef] [PubMed]
- Wu, T.D.; Watanabe, C.K. GMAP: A Genomic Mapping and Alignment Program for mRNA and EST Sequences. Bioinformatics 2005, 21, 1859–1875. [Google Scholar] [CrossRef]
- Duan, J.; Li, S.; Zhang, Z.; Yao, L.; Yang, X.; Ma, S.; Duan, N.; Wang, J.; Zhu, X.; Zhao, P. A Transcriptional Atlas of the Silk Gland in Antheraea pernyi Revealed by IsoSeq. J. Asia-Pac. Entomol. 2023, 26, 102043. [Google Scholar] [CrossRef]
- Buchfink, B.; Xie, C.; Huson, D.H. Fast and Sensitive Protein Alignment Using DIAMOND. Nat. Methods 2015, 12, 59–60. [Google Scholar] [CrossRef]
- Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T.; et al. Gene Ontology: Tool for the Unification of Biology. Nat. Genet. 2000, 25, 25–29. [Google Scholar] [CrossRef]
- SWISS-PROT: Connecting Biomolecular Knowledge via a Protein Database. Curr. Issues Mol. Biol. 2001, 3, 47–55. [CrossRef]
- Tatusov, R.L.; Fedorova, N.D.; Jackson, J.D.; Jacobs, A.R.; Kiryutin, B.; Koonin, E.V.; Krylov, D.M.; Mazumder, R.; Mekhedov, S.L.; Nikolskaya, A.N.; et al. The COG Database: An Updated Version Includes Eukaryotes. BMC Bioinf. 2003, 4, 41. [Google Scholar] [CrossRef]
- Bu, D.; Luo, H.; Huo, P.; Wang, Z.; Zhang, S.; He, Z.; Wu, Y.; Zhao, L.; Liu, J.; Guo, J.; et al. KOBAS-i: Intelligent Prioritization and Exploratory Visualization of Biological Functions for Gene Enrichment Analysis. Nucleic Acids Res. 2021, 49, W317–W325. [Google Scholar] [CrossRef] [PubMed]
- Kanehisa, M. The KEGG Resource for Deciphering the Genome. Nucleic Acids Res. 2004, 32, D277–D280. [Google Scholar] [CrossRef] [PubMed]
- Kong, L.; Zhang, Y.; Ye, Z.-Q.; Liu, X.-Q.; Zhao, S.-Q.; Wei, L.; Gao, G. CPC: Assess the Protein-Coding Potential of Transcripts Using Sequence Features and Support Vector Machine. Nucleic Acids Res. 2007, 35, W345–W349. [Google Scholar] [CrossRef]
- Sun, L.; Luo, H.; Bu, D.; Zhao, G.; Yu, K.; Zhang, C.; Liu, Y.; Chen, R.; Zhao, Y. Utilizing Sequence Intrinsic Composition to Classify Protein-Coding and Long Non-Coding Transcripts. Nucleic Acids Res. 2013, 41, e166. [Google Scholar] [CrossRef]
- Wang, L.; Park, H.J.; Dasari, S.; Wang, S.; Kocher, J.-P.; Li, W. CPAT: Coding-Potential Assessment Tool Using an Alignment-Free Logistic Regression Model. Nucleic Acids Res. 2013, 41, e74. [Google Scholar] [CrossRef]
- Li, A.; Zhang, J.; Zhou, Z. PLEK: A Tool for Predicting Long Non-Coding RNAs and Messenger RNAs Based on an Improved k-Mer Scheme. BMC Bioinf. 2014, 15, 311. [Google Scholar] [CrossRef]
- Shang, X.; Cao, Y.; Ma, L. Alternative Splicing in Plant Genes: A Means of Regulating the Environmental Fitness of Plants. Int. J. Mol. Sci. 2017, 18, 432. [Google Scholar] [CrossRef]
- Arora, A.; Goering, R.; Lo, H.Y.G.; Lo, J.; Moffatt, C.; Taliaferro, J.M. The Role of Alternative Polyadenylation in the Regulation of Subcellular RNA Localization. Front. Genet. 2022, 12, 818668. [Google Scholar] [CrossRef] [PubMed]
- Foissac, S.; Sammeth, M. ASTALAVISTA: Dynamic and Flexible Analysis of Alternative Splicing Events in Custom Gene Datasets. Nucleic Acids Res. 2007, 35, W297–W299. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Ghany, S.E.; Hamilton, M.; Jacobi, J.L.; Ngam, P.; Devitt, N.; Schilkey, F.; Ben-Hur, A.; Reddy, A.S.N. A Survey of the Sorghum Transcriptome Using Single-Molecule Long Reads. Nat. Commun. 2016, 7, 11706. [Google Scholar] [CrossRef]
- Mistry, J.; Finn, R.D.; Eddy, S.R.; Bateman, A.; Punta, M. Challenges in Homology Search: HMMER3 and Convergent Evolution of Coiled-Coil Regions. Nucleic Acids Res. 2013, 41, e121. [Google Scholar] [CrossRef]
- Li, X.-S.; Wang, G.-B.; Sun, Y.; Liu, W.; He, Y.-Z.; Wang, F.-C.; Jiang, Y.-R.; Qin, L. Transcriptome Analysis of the Midgut of the Chinese Oak Silkworm Antheraea pernyi Infected with Antheraea pernyi Nucleopolyhedrovirus. PLoS ONE 2016, 11, e0165959. [Google Scholar] [CrossRef] [PubMed]
- Love, M.I.; Huber, W.; Anders, S. Moderated Estimation of Fold Change and Dispersion for RNA-Seq Data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef]
- Pu, S.; Fang, Y.; Yang, Y.; Qu, Q.; Liu, M.; Lian, J.; Tang, X.; Shen, Z.; Qian, P. Identification of Long Non-Coding RNAs in Response to Microsporidia Infection in Silkworm. Bombyx mori. J. Econ. Entomol. 2024, 117, 772–781. [Google Scholar] [CrossRef]
- Wu, Y.; Cheng, T.; Liu, C.; Liu, D.; Zhang, Q.; Long, R.; Zhao, P.; Xia, Q. Systematic Identification and Characterization of Long Non-Coding RNAs in the Silkworm. Bombyx mori. PLoS ONE 2016, 11, e0147147. [Google Scholar] [CrossRef]
- Lin, S.; Zhang, S.L.; Yin, H.T.; Zhao, Z.M.; Chen, Z.K.; Shen, M.M.; Zhang, Z.D.; Guo, X.J.; Wu, P. Cellular Lnc_209997 Suppresses Bombyx mori Nucleopolyhedrovirus Replication by Targeting miR-275-5p in B. Mori. Insect Mol. Biol. 2022, 31, 308–316. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Cheng, T.; Xu, P.; Fang, T.; Xia, Q. Bombyx mori Transcription Factors: Genome-Wide Identification, Expression Profiles and Response to Pathogens by Microarray Analysis. J. Insect Sci. 2012, 12, 40. [Google Scholar] [CrossRef] [PubMed]
- Ma, Y.; Sun, Q.; Huang, L.; Luo, Q.; Zeng, W.; Ou, Y.; Ma, J.; Xu, H. Genome-Wide Survey and Characterization of Transcription Factors in the Silk Gland of the Silkworm, Bombyx mori. PLoS ONE 2021, 16, e0259870. [Google Scholar] [CrossRef]
- Kelemen, O.; Convertini, P.; Zhang, Z.; Wen, Y.; Shen, M.; Falaleeva, M.; Stamm, S. Function of Alternative Splicing. Gene 2013, 514, 1–30. [Google Scholar] [CrossRef] [PubMed]
- Marasco, L.E.; Kornblihtt, A.R. The Physiology of Alternative Splicing. Nat. Rev. Mol. Cell Biol. 2023, 24, 242–254. [Google Scholar] [CrossRef]
- Tian, B.; Manley, J.L. Alternative Polyadenylation of mRNA Precursors. Nat. Rev. Mol. Cell Biol. 2017, 18, 18–30. [Google Scholar] [CrossRef]
- Kang, X.; Wang, Y.; Liang, W.; Tang, X.; Zhang, Y.; Wang, L.; Zhao, P.; Lu, Z. Bombyx mori Nucleopolyhedrovirus Downregulates Transcription Factor BmFoxO to Elevate Virus Infection. Dev. Comp. Immunol. 2021, 116, 103904. [Google Scholar] [CrossRef]
- Zhou, L.; Dang, Z.; Wang, S.; Li, S.; Zou, Y.; Zhao, P.; Xia, Q.; Lu, Z. Transcription Factor STAT Enhanced Antimicrobial Activities in Bombyx mori. Int. J. Biol. Macromol. 2024, 254, 127637. [Google Scholar] [CrossRef]
- Yu, S.; Luo, F.; Xu, Y.; Zhang, Y.; Jin, L.H. Drosophila Innate Immunity Involves Multiple Signaling Pathways and Coordinated Communication between Different Tissues. Front. Immunol. 2022, 13, 905370. [Google Scholar] [CrossRef]
- Chen, C.; Yang, L.; Abbas, M.N.; Zou, D.; Li, J.; Geng, X.; Zhang, H.; Sun, Y. Relish Regulates Innate Immunity via Mediating ATG5 Activity in Antheraea pernyi. Dev. Comp. Immunol. 2022, 132, 104406. [Google Scholar] [CrossRef]
- Araujo, P.R.; Yoon, K.; Ko, D.; Smith, A.D.; Qiao, M.; Suresh, U.; Burns, S.C.; Penalva, L.O.F. Before It Gets Started: Regulating Translation at the 5′ UTR. Comp. Funct. Genom. 2012, 2012, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Ryczek, N.; Łyś, A.; Makałowska, I. The Functional Meaning of 5′UTR in Protein-Coding Genes. Int. J. Mol. Sci. 2023, 24, 2976. [Google Scholar] [CrossRef]
- Tanaka, H.; Matsuki, H.; Furukawa, S.; Sagisaka, A.; Kotani, E.; Mori, H.; Yamakawa, M. Identification and Functional Analysis of Relish Homologs in the Silkworm, Bombyx mori. Biochim. Biophys. Acta (BBA)-Gene Struct. Expr. 2007, 1769, 559–568. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Han, S.; Jin, K.; Yu, T.; Chen, H.; Zhou, X.; Tan, Z.; Zhang, G. SOCS2 Suppresses Inflammation and Apoptosis during NASH Progression through Limiting NF-κB Activation in Macrophages. Int. J. Biol. Sci. 2021, 17, 4165–4175. [Google Scholar] [CrossRef] [PubMed]
- Yuan, Y.; Zhu, F.; Xiao, R.; Ge, Q.; Tang, H.; Kong, M.; Taha, R.H.; Chen, K. Increased Expression of Suppressor of Cytokine Signaling 2 (BmSOCS2) Is Correlated with Suppression of Bombyx mori Nucleopolyhedrovirus Replication in Silkworm Larval Tissues and Cells. J. Invertebr. Pathol. 2020, 174, 107419. [Google Scholar] [CrossRef]
- Kausar, S.; Gul, I.; Liu, R.; Ke, X.-X.; Dong, Z.; Abbas, M.N.; Cui, H. Antheraea pernyi Suppressor of Cytokine Signaling 2 Negatively Modulates the JAK/STAT Pathway to Attenuate Microbial Infection. Int. J. Mol. Sci. 2022, 23, 10389. [Google Scholar] [CrossRef]
- Abbas, M.N.; Kausar, S.; Zhao, E.; Cui, H. Suppressors of Cytokine Signaling Proteins as Modulators of Development and Innate Immunity of Insects. Dev. Comp. Immunol. 2020, 104, 103561. [Google Scholar] [CrossRef]
- Babon, J.J.; Sabo, J.K.; Zhang, J.-G.; Nicola, N.A.; Norton, R.S. The SOCS Box Encodes a Hierarchy of Affinities for Cullin5: Implications for Ubiquitin Ligase Formation and Cytokine Signalling Suppression. J. Mol. Biol. 2009, 387, 162–174. [Google Scholar] [CrossRef] [PubMed]
- Zhang, X.; Wang, Q.; Cui, M.; Zhang, C.; Wu, Y.; Xia, H. Molecular Identification of Suppressor of Cytokine Signaling 2 (SOCS2) and Its Response to BmNPV in Bombyx mori (Lepidoptera: Bombycidae). J. Asia-Pac. Entomol. 2024, 27, 102226. [Google Scholar] [CrossRef]
- Jia, L.; Mao, Y.; Ji, Q.; Dersh, D.; Yewdell, J.W.; Qian, S.-B. Decoding mRNA Translatability and Stability from the 5′ UTR. Nat. Struct. Mol. Biol. 2020, 27, 814–821. [Google Scholar] [CrossRef]
- Choi, Y.; Bowman, J.W.; Jung, J.U. Autophagy during Viral Infection-a Double-Edged Sword. Nat. Rev. Microbiol. 2018, 16, 341–354. [Google Scholar] [CrossRef]
- Chen, T.; Tu, S.; Ding, L.; Jin, M.; Chen, H.; Zhou, H. The Role of Autophagy in Viral Infections. J. Biomed. Sci. 2023, 30, 5. [Google Scholar] [CrossRef]
- Heaton, N.S.; Randall, G. Dengue Virus and Autophagy. Viruses 2011, 3, 1332–1341. [Google Scholar] [CrossRef]
- Li, J.; Liu, Y.; Wang, Z.; Liu, K.; Wang, Y.; Liu, J.; Ding, H.; Yuan, Z. Subversion of Cellular Autophagy Machinery by Hepatitis B Virus for Viral Envelopment. J. Virol. 2011, 85, 6319–6333. [Google Scholar] [CrossRef]
- Fei, S.; Xia, J.; Mehmood, N.; Wang, Y.; Feng, M.; Sun, J. Autophagy Promotes Replication of Bombyx mori Nucleopolyhedrovirus in Insect Cells. Int. J. Biol. Macromol. 2024, 277, 134325. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Xiao, Q.; Zhou, X.-L.; Zhu, Y.; Dong, Z.-Q.; Chen, P.; Pan, M.-H.; Lu, C. Bombyx mori Nuclear Polyhedrosis Virus (BmNPV) Induces Host Cell Autophagy to Benefit Infection. Viruses 2017, 10, 14. [Google Scholar] [CrossRef] [PubMed]
- Barber, G.N. Host Defense, Viruses and Apoptosis. Cell Death Differ. 2001, 8, 113–126. [Google Scholar] [CrossRef]
- Hardwick, J.M. Virus-Induced Apoptosis. In Advances in Pharmacology; Kaufmann, S.H., Ed.; Apoptosls; Academic Press: Cambridge, MA, USA, 1997; Volume 41, pp. 295–336. [Google Scholar]
- Ampomah, P.B.; Lim, L.H.K. Influenza a Virus-Induced Apoptosis and Virus Propagation. Apoptosis 2020, 25, 1–11. [Google Scholar] [CrossRef]
- Yuan, S.; Zhang, N.; Xu, L.; Zhou, L.; Ge, X.; Guo, X.; Yang, H. Induction of Apoptosis by the Nonstructural Protein 4 and 10 of Porcine Reproductive and Respiratory Syndrome Virus. PLoS ONE 2016, 11, e0156518. [Google Scholar] [CrossRef]
- Kash, J.C.; Goodman, A.G.; Korth, M.J.; Katze, M.G. Hijacking of the Host-Cell Response and Translational Control during Influenza Virus Infection. Virus Res. 2006, 119, 111–120. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.-W.; Wang, S.-S.; Chen, L.-Y.; Huang, H.-Y.; He, S.; Hung, C.-H.; Lin, C.-L.; Chang, P.-J. Interaction and Assembly of the DNA Replication Core Proteins of Kaposi’s Sarcoma-Associated Herpesvirus. Microbiol. Spectrum 2023, 11, e02254-23. [Google Scholar] [CrossRef]
- Kirby, M.P.; Stevenson, C.; Worrall, L.J.; Chen, Y.; Young, C.; Youm, J.; Strynadka, N.C.J.; Allan, D.W.; Jan, E. The Hinge Region of the Israeli Acute Paralysis Virus Internal Ribosome Entry Site Directs Ribosomal Positioning, Translational Activity, and Virus Infection. J. Virol. 2022, 96, e01330-21. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Z.; Ruan, S.; Li, Y.; Qi, T.; Qi, Y.; Huang, Y.; Liu, Z.; Ruan, Q.; Ma, Y. The Influence of Extra-Ribosomal Functions of Eukaryotic Ribosomal Proteins on Viral Infection. Biomolecules 2024, 14, 1565. [Google Scholar] [CrossRef] [PubMed]
- Miller, C.M.; Selvam, S.; Fuchs, G. Fatal Attraction: The Roles of Ribosomal Proteins in the Viral Life Cycle. WIREs RNA 2021, 12, e1613. [Google Scholar] [CrossRef]
- Dove, B.K.; You, J.-H.; Reed, M.L.; Emmett, S.R.; Brooks, G.; Hiscox, J.A. Changes in Nucleolar Morphology and Proteins during Infection with the Coronavirus Infectious Bronchitis Virus. Cell. Microbiol. 2006, 8, 1147–1157. [Google Scholar] [CrossRef]
- Emmott, E.; Smith, C.; Emmett, S.R.; Dove, B.K.; Hiscox, J.A. Elucidation of the Avian Nucleolar Proteome by Quantitative Proteomics Using SILAC and Changes in Cells Infected with the Coronavirus Infectious Bronchitis Virus. Proteomics 2010, 10, 3558–3562. [Google Scholar] [CrossRef]
- Wu, W.; Wang, C.; Xia, C.; Liu, S.; Mei, Q. MicroRNA Let-7 Suppresses Influenza a Virus Infection by Targeting RPS16 and Enhancing Type I Interferon Response. Front. Cell. Infect. Microbiol. 2022, 12, 904775. [Google Scholar] [CrossRef]
- Taracena, M.L.; Bottino-Rojas, V.; Talyuli, O.A.C.; Walter-Nuno, A.B.; Oliveira, J.H.M.; Angleró-Rodriguez, Y.I.; Wells, M.B.; Dimopoulos, G.; Oliveira, P.L.; Paiva-Silva, G.O. Regulation of Midgut Cell Proliferation Impacts Aedes aegypti Susceptibility to Dengue Virus. PLoS Negl. Trop. Dis. 2018, 12, e0006498. [Google Scholar] [CrossRef]
- Greber, B.J.; Ban, N. Structure and Function of the Mitochondrial Ribosome. Annu. Rev. Biochem. 2016, 85, 103–132. [Google Scholar] [CrossRef]
- De Silva, D.; Tu, Y.-T.; Amunts, A.; Fontanesi, F.; Barrientos, A. Mitochondrial Ribosome Assembly in Health and Disease. Cell Cycle 2015, 14, 2226–2250. [Google Scholar] [CrossRef] [PubMed]
- Nadler, F.; Lavdovskaia, E.; Richter-Dennerlein, R. Maintaining Mitochondrial Ribosome Function: The Role of Ribosome Rescue and Recycling Factors. RNA Biol. 2022, 19, 117–131. [Google Scholar] [CrossRef] [PubMed]
- Hinton, A.; Bond, S.; Forgac, M. V-ATPase Functions in Normal and Disease Processes. Pflüg. Arch.-Eur. J. Physiol. 2009, 457, 589–598. [Google Scholar] [CrossRef]
- Neupane, P.; Bhuju, S.; Thapa, N.; Bhattarai, H.K. ATP Synthase: Structure, Function and Inhibition. Biomol. Concepts 2019, 10, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Lü, P.; Xia, H.; Gao, L.; Pan, Y.; Wang, Y.; Cheng, X.; Lü, H.; Lin, F.; Chen, L.; Yao, Q.; et al. V-ATPase Is Involved in Silkworm Defense Response against Bombyx mori Nucleopolyhedrovirus. PLoS ONE 2013, 8, e64962. [Google Scholar] [CrossRef]
Total Bases (Gbp) | Total Number | Minimum Length (bp) | Average Length (bp) | Maximum Length (bp) | N50 (bp) | |
Raw reads | 39.48 | 550,771 | 57 | 71,679 | 358,048 | 128,749 |
Subreads | 38.01 | 19,093,122 | 51 | 1991 | 223,063 | 2269 |
CCS | 0.79 | 378,156 | 109 | 2081 | 14,486 | 2321 |
FLNC with ploy(A) | 0.55 | 288,759 | 57 | 1888 | 9624 | 2113 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, X.; Li, Y.; Yang, X.; Zhu, X.; Meng, F.; Zhang, Y.; Duan, J. Integrating Full-Length and Second-Generation Transcriptomes to Elucidate the ApNPV-Induced Transcriptional Reprogramming in Antheraea pernyi Midgut. Insects 2025, 16, 792. https://doi.org/10.3390/insects16080792
Liu X, Li Y, Yang X, Zhu X, Meng F, Zhang Y, Duan J. Integrating Full-Length and Second-Generation Transcriptomes to Elucidate the ApNPV-Induced Transcriptional Reprogramming in Antheraea pernyi Midgut. Insects. 2025; 16(8):792. https://doi.org/10.3390/insects16080792
Chicago/Turabian StyleLiu, Xinlei, Ying Li, Xinfeng Yang, Xuwei Zhu, Fangang Meng, Yaoting Zhang, and Jianping Duan. 2025. "Integrating Full-Length and Second-Generation Transcriptomes to Elucidate the ApNPV-Induced Transcriptional Reprogramming in Antheraea pernyi Midgut" Insects 16, no. 8: 792. https://doi.org/10.3390/insects16080792
APA StyleLiu, X., Li, Y., Yang, X., Zhu, X., Meng, F., Zhang, Y., & Duan, J. (2025). Integrating Full-Length and Second-Generation Transcriptomes to Elucidate the ApNPV-Induced Transcriptional Reprogramming in Antheraea pernyi Midgut. Insects, 16(8), 792. https://doi.org/10.3390/insects16080792