Skip to main content
Log in

Transcriptome-wide analysis of the difference of alternative splicing in susceptible and resistant silkworm strains after BmNPV infection

3 Biotech Aims and scope Submit manuscript

Abstract

Novel alternative splicing events were identified from BmNPV-susceptible and -resistant silkworm strains after BmNPV infection using high-throughput RNA-sequencing strategy. In total, 12.82 Gb clean RNA-seq data were generated for the two midgut samples from BmNPV-susceptible and -resistant silkworm strains, and 14.78 Gb clean data for the two fat body samples. The number of alternative splicing events and isoforms in the BmNPV-susceptible silkworm strain was more than that in the BmNPV-resistant silkworm strain. Furthermore, alternative splicing genes uniquely present in BmNPV-resistant silkworm strain were involved in functions about ribosome, whereas, alternative splicing genes uniquely present in BmNPV-susceptible silkworm strain were implicated in functions like DNA helicase activity and signal transduction. Additionally, 33 expressed SR or SR-like proteins were identified, and three genes encoding SR or SR-like proteins (tetratricopeptide repeat protein 14 homolog, ubiquitin carboxyl-terminal hydrolase 32 and zinc finger CCCH domain-containing protein 18) have a higher number of different alternative splicing events between two silkworm strains. The present study suggested BmNPV treatment may have a smaller effect on the mRNA transcription in BmNPV-resistant silkworms than that in BmNPV-susceptible silkworms, and functions of alternative splicing genes are different between the two silkworm strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Andreeva A (2013) Identification of some proteins of blood and tissue fluid in fish with undeciphered genome. Zh Evol Biokhim Fiziol 49:394–402

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300

    Google Scholar 

  • Consortium GO (2015) Gene ontology consortium: going forward. Nucleic Acids Res 43:D1049–D1056

    Google Scholar 

  • Graveley BR (2001) Alternative splicing: increasing diversity in the proteomic world. Trends Genetics 17:100–107

    Google Scholar 

  • Huang L, Cheng T, Xu P, Cheng D, Fang T, Xia Q (2009) A genome-wide survey for host response of silkworm, Bombyx mori during pathogen Bacillus bombyseptieus infection. PLoS One 4:e8098

    Google Scholar 

  • Hussain M, Asgari S (2014) MicroRNAs as mediators of insect host–pathogen interactions and immunity. J Insect Physiol 70:151–158

    Google Scholar 

  • Kang L et al (2011) Arginine kinase is highly expressed in a resistant strain of silkworm (Bombyx mori, Lepidoptera): Implication of its role in resistance to Bombyx mori nucleopolyhedrovirus. Comp Biochem Physiol B Biochem Mol Biol 158:230–234

    Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Google Scholar 

  • Lekha G, Gupta T, Awasthi AK, Murthy GN, Trivedy K, Ponnuvel KM (2015) Genome wide microarray based expression profiles associated with BmNPV resistance and susceptibility in Indian silkworm races of Bombyx mori. Genomics 106:393–403

    Google Scholar 

  • Li G, Qian H, Luo X, Xu P, Yang J, Liu M, Xu A (2016) Transcriptomic analysis of resistant and susceptible Bombyx mori strains following BmNPV infection provides insights into the antiviral mechanisms. Int J Genomics 2016:2086346. https://doi.org/10.1155/2016/2086346

    Google Scholar 

  • Long JC, Caceres JF (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417:15–27

    Google Scholar 

  • Morishima I, Yamano Y, Inoue K, Matsuo N (1997) Eicosanoids mediate induction of immune genes in the fat body of the silkworm, Bombyx mori. FEBS Lett 419:83–86

    Google Scholar 

  • Niu Y-s, Wang M-x, Liang S, Zhou F, Miao Y-g (2012) Expression and localization of silkworm adaptor protein complex-1 subunits, which were down-regulated post baculovirus infection. Mol Biol Rep 39:10775–10783

    Google Scholar 

  • Preacher KJ, Briggs NE (2001) Calculation for Fisher’s exact test: an interactive calculation tool for Fisher’s exact probability test for 2 x 2 tables [Computer software]. Available from http://quantpsy.org

  • Qin L et al (2012) Comparative proteomic analysis reveals that caspase-1 and serine protease may be involved in silkworm resistance to Bombyx mori nuclear polyhedrosis virus. J Proteom 75:3630–3638

    Google Scholar 

  • Sanford J, Ellis J, Caceres J (2005) Multiple roles of arginine/serine-rich splicing factors in RNA processing. Biochem Soc Trans 33:443–446

    Google Scholar 

  • Shao W et al (2012) Alternative splicing and trans-splicing events revealed by analysis of the Bombyx mori transcriptome. RNA 18:1395–1407

    Google Scholar 

  • Slack J, Arif BM (2007) The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 69:100

    Google Scholar 

  • Trapnell C et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protocols 7:562–578

    Google Scholar 

  • Xu A, Lin C, Qian H, Sun P, Zhang Y, Liu M, Li L (2013) Breeding of a new silkworm variety “Huakang 2” with tolerance to Bombyx mori nucleopolyhedrovirus disease. Sci Seric 39:275–282

    Google Scholar 

  • Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16:284–287

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31802136); the China Agriculture Research System (Sericulture industry, CARS-18); The Natural Science Foundation of the Jiangsu Higher Education Institutions of China (17KJB230001); Key Research & Development program of Zhenjiang (NY2018021, NY2017017).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Heying Qian or Anying Xu.

Ethics declarations

Conflict of interest

The authors declares that they have no conflict interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13205_2019_1669_MOESM1_ESM.xlsx

T01.AltSplice_info: the alternative splicing information of the fat body of Qiufeng that is susceptible to BmNPV (XLSX 406 KB)

13205_2019_1669_MOESM2_ESM.xlsx

T02.AltSplice_info: the alternative splicing information of the fat body of QiufengN that is resistant to BmNPV (XLSX 314 KB)

13205_2019_1669_MOESM3_ESM.xlsx

T03.AltSplice_info: the alternative splicing information of the midgut of Qiufeng that is susceptible to BmNPV (XLSX 341 KB)

13205_2019_1669_MOESM4_ESM.xlsx

T04.AltSplice_info: the alternative splicing information of the midgut of QiufengN that is resistant to BmNPV (XLSX 331 KB)

T05. Alternative splicing events common between F1, F2, M1, M2 (XLSX 56 KB)

13205_2019_1669_MOESM6_ESM.docx

Table S1 The enriched Gene Ontology terms of FAS-genes and MAS-genes. Table S2 The enriched Gene Ontology terms of RAS-genes and SAS-genes. Table S3 Primers of 10 AS-genes of qRT-PCR (DOCX 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, G., Zhou, K., Zhao, G. et al. Transcriptome-wide analysis of the difference of alternative splicing in susceptible and resistant silkworm strains after BmNPV infection. 3 Biotech 9, 152 (2019). https://doi.org/10.1007/s13205-019-1669-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-019-1669-9

Keywords

Navigation