Advertisement

Virologica Sinica

, Volume 33, Issue 4, pp 345–358 | Cite as

Insights into the Temporal Gene Expression Pattern in Lymantria dispar Larvae During the Baculovirus Induced Hyperactive Stage

  • Upendra Raj Bhattarai
  • Mandira Katuwal Bhattarai
  • Fengjiao Li
  • Dun Wang
Research Article

Abstract

Baculoviruses are effective biological control agents for many insect pests. They not only efficiently challenge the host immune system but also make them hyperactive for better virus dispersal. Some investigations have focused on the viral mechanisms for induction of such altered response from the host. However, there are no current studies monitoring changes in gene expression during this altered phenotype in infected larvae. The L. dispar multiple nucleopolyhedrovirus (LdMNPV) induces hyperactivity in third instar L. dispar larvae at 3-days post infection (dpi), to continued till 6 dpi. The transcriptome profiles of the infected and uninfected larvae at these time points were analyzed to provide new clues on the response of the larvae towards infection during hyperactivity. Gene ontology enrichment analysis revealed, most of the differentially expressed genes (DEGs) were involved in proteolysis, extracellular region, and serine-type endopeptidase activity. Similarly, Kyoto Encyclopedia of Genes and Genome enrichment analysis showed maximum enrichment of 487 genes of the signal transduction category and neuroactive ligand–receptor interaction sub-category with 85 annotated genes. In addition, enrichment map visualization of gene set enrichment analysis showed the coordinated response of neuroactive ligand–receptor interaction genes with other functional gene sets, as an important signal transduction mechanism during the hyperactive stage. Interestingly all the DEGs in neuroactive ligand–receptor interactions were serine proteases, their differential expression during the hyperactive stage correlated with their conceivable involvement in disease progression and the resulting altered phenotype during this period. The outcome provides a basic understanding of L. dispar larval responses to LdMNPV infection during the hyperactive stage and helps to determine the important host factors involved in this process.

Keywords

Gypsy moth Lymantria dispar multiple nucleopolyhedrovirus (LdMNPV) Hyperactivity Gene expression pattern 

Notes

Acknowledgements

We thank Professor Liang-Jian Qu from the Chinese Academy of Forestry, Beijing, China, for generously providing gypsy moth eggs and LdMNPV. We also thank Dr. Huan Yu from Hunan Agricultural University for her inputs during experimental design. We would like to acknowledge Professor Christopher Rensing from Fujian Agriculture & Forestry University and Asst. Professor Dr. Xiangfeng Jing from Northwest A&F University for reviewing the manuscript. This study was supported by NSFC Grant (31670659), Special Fund for Forest Scientific Research in the Public Welfare (201404403-09) and Shaanxi Provincial Science and Technology Innovation Project (2014KTCL02-14).

Author Contributions

Research design by DW, URB, the experiments were conducted by MKB, URB, LF, data were analyzed by URB, MKB, materials and lab conditions were provided by DW, Manuscript was written by URB, MKB, DW.

Compliance with Ethics Guidelines

Conflict of interest

The authors declare that they have no conflict of interest.

Animal and Human Rights Statement

All institutional and national guidelines for the care and use of laboratory animals were followed.

Supplementary material

12250_2018_46_MOESM1_ESM.docx (548 kb)
Supplementary material 1 (DOCX 547 kb)

References

  1. Ainsley JA, Pettus JM, Bosenko D, Gerstein CE, Zinkevich N, Anderson MG, Adams CM, Welsh MJ, Johnson WA (2003) Enhanced locomotion caused by loss of the Drosophila DEG/ENaC protein pickpocket1. Curr Biol 13:1557–1563CrossRefPubMedGoogle Scholar
  2. Alalouni U, Schädler M, Brandl R (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J Appl Entomol 137:721–738CrossRefGoogle Scholar
  3. Appel LF, Prout M, Abu-Shumays R, Hammonds A, Garbe JC, Fristrom D, Fristrom J (1993) The Drosophila Stubble-stubbloid gene encodes an apparent transmembrane serine protease required for epithelial morphogenesis. Proc Natl Acad Sci U S A 90:4937–4941CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bayer CA, Halsell SR, Fristrom JW, Kiehart DP, Von Kalm L (2003) Genetic interactions between the RhoA and Stubble-stubbloid loci suggest a role for a type II transmembrane serine protease in intracellular signaling during Drosophila imaginal disc morphogenesis. Genetics 165:1417–1432PubMedPubMedCentralGoogle Scholar
  5. Buckmann D, Tomaschko KH (1992) 20-hydroxyecdysone stimulates molting in pycnogonid larvae (arthropoda, pantopoda). Gen Comp Endocrinol 88:261–266CrossRefPubMedGoogle Scholar
  6. Cai M, Zhao W, Jing Y, Song Q, Zhang X, Wang J, Zhao X (2016) 20-Hydroxyecdysone activates Forkhead box O to promote proteolysis during Helicoverpa armigera molting. Development 143:1005–1015CrossRefPubMedGoogle Scholar
  7. Cory JS, Clarke EE, Brown ML, Hails RS, O’Reilly DR (2004) Microparasite manipulation of an insect: the influence of the egt gene on the interaction between a baculovirus and its lepidopteran host. Funct Ecol 18:443–450CrossRefGoogle Scholar
  8. Danneels EL, Van Vaerenbergh M, Debyser G, Devreese B, de Graaf DC (2015) Honeybee venom proteome profile of queens and winter bees as determined by a mass spectrometric approach. Toxins 7:4468–4483CrossRefPubMedPubMedCentralGoogle Scholar
  9. Debski KJ, Pitkanen A, Puhakka N, Bot AM, Khurana I, Harikrishnan KN, Ziemann M, Kaspi A, Elosta A, Lukasiuk K (2016) Etiology matters—genomic DNA methylation patterns in three rat models of acquired epilepsy. Sci Rep 6:25668CrossRefPubMedPubMedCentralGoogle Scholar
  10. Di Cera E (2009) Serine proteases. IUBMB life 61:510–515CrossRefPubMedPubMedCentralGoogle Scholar
  11. Etebari K, Hegde S, Saldaña MA, Widen SG, Wood TG, Asgari S, Hughes GL (2017) Global transcriptome analysis of Aedes aegypti mosquitoes in response to Zika virus infection. mSphere 2:e00456-17CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fan B, Wu TD, Li W, Kirchhofer D (2005) Identification of hepatocyte growth factor activator inhibitor-1B as a potential physiological inhibitor of prostasin. J Biol Chem 280:34513–34520CrossRefPubMedGoogle Scholar
  13. Fredericksen MA, Zhang Y, Hazen ML, Loreto RG, Mangold CA, Chen DZ, Hughes DP (2017) Three-dimensional visualization and a deep-learning model reveal complex fungal parasite networks in behaviorally manipulated ants. Proc Natl Acad Sci U S A 114:12590–12595CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gorczyca D, Younger S, Meltzer S, Kim SE, Cheng L, Song W, Lee HY, Jan LY, Jan YN (2014) Identification of Ppk26, a DEG/ENaC channel functioning with Ppk1 in a mutually dependent manner to guidelocomotion behavior in Drosophila. Cell Rep 9:1446–1458CrossRefPubMedPubMedCentralGoogle Scholar
  15. Goulson D (1997) Wipfelkrankheit: modification of host behaviour during baculoviral infection. Oecologia 109:219–228CrossRefPubMedGoogle Scholar
  16. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  17. Grove MJ, Hoover K (2007) Intrastadial developmental resistance of third instar gypsy moths (Lymantria dispar L.) to L. dispar nucleopolyhedrovirus. Biol Control 40:355–361CrossRefGoogle Scholar
  18. Grzywacz D (2017) Basic and applied research: Baculovirus. In: Lacey LA (ed) Microbial control of insect and mite pests. Academic Press, London, pp 27–46CrossRefGoogle Scholar
  19. Hecht PM, Anderson KV (1992) Extracellular proteases and embryonic pattern formation. Trends Cell Biol 2:197–202CrossRefPubMedGoogle Scholar
  20. Hooper JD, Clements JA, Quigley JP, Antalis TM (2001) Type II transmembrane serine proteases. Insights into an emerging class of cell surface proteolytic enzymes. J Biol Chem 276:857–860CrossRefPubMedGoogle Scholar
  21. Hoover K, Grove MJ (2009) Specificity of developmental resistance in gypsy moth (Lymantria dispar) to two DNA-insect viruses. Virol Sin 24:493–500CrossRefGoogle Scholar
  22. Hoover K, Grove M, Gardner M, Hughes DP, McNeil J, Slavicek J (2011) A gene for an extended phenotype. Science 333:1401CrossRefPubMedGoogle Scholar
  23. Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, Kobayashi M, Maeda S, Hammock BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci U S A 102:2584–2589CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lemaitre B, Nicolas E, Michaut L, Reichhart J-M, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–983CrossRefPubMedGoogle Scholar
  25. Lemosy EK, Hong CC, Hashimoto C (1999) Signal transduction by a protease cascade. Trends Cell Biol 9:102–107CrossRefPubMedGoogle Scholar
  26. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323CrossRefGoogle Scholar
  27. Lin CY, Anders J, Johnson M, Dickson RB (1999) Purification and characterization of a complex containing matriptase and a kunitz-type serine protease inhibitor from human milk. J Biol Chem 274:18237–18242CrossRefPubMedGoogle Scholar
  28. Lin H, Xia X, Yu L, Vasseur L, Gurr GM, Yao F, Yang G, You M (2015) Genome-wide identification and expression profiling of serine proteases and homologs in the diamondback moth, Plutella xylostella (L.). BMC Genom 16:1054CrossRefGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  30. Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:986–996CrossRefGoogle Scholar
  31. Markland FS Jr (1991) Inventory of alpha- and beta-fibrinogenases from snake venoms. For the Subcommittee on Nomenclature of Exogenous Hemostatic Factors of the Scientific and Standardization Committee of the International Society on Thrombosis and Haemostasis. Thromb Haemost 65:438–443CrossRefPubMedGoogle Scholar
  32. McEnery MW, Siegel RE (2014) Neurotransmitter receptors. In: Aminoff MJ, Daroff RB (eds) Encyclopedia of the neurological sciences, vol 2. Academic Press, Oxford, pp 552–564CrossRefGoogle Scholar
  33. Merico D, Isserlin R, Stueker O, Emili A, Bader GD (2010) Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS ONE 5:e13984CrossRefPubMedPubMedCentralGoogle Scholar
  34. Mirth C (2005) Ecdysteroid control of metamorphosis in the differentiating adult leg structures of Drosophila melanogaster. Dev Biol 278:163–174CrossRefPubMedGoogle Scholar
  35. Mobashir M, Schraven B, Beyer T (2012) Simulated evolution of signal transduction networks. PLoS ONE 7:e50905CrossRefPubMedPubMedCentralGoogle Scholar
  36. Oberemok VV, Laikova KV, Zaitsev AS, Gushchin VA, Skorokhod OA (2016) The RING for gypsy moth control: topical application of fragment of its nuclear polyhedrosis virus anti-apoptosis gene as insecticide. Pestic Biochem Phys 131:32–39CrossRefGoogle Scholar
  37. O’Reilly D, Miller L (1989) A baculovirus blocks insect molting by producing ecdysteroid UDP-glucosyl transferase. Science 245:1110–1112CrossRefPubMedGoogle Scholar
  38. Ovaere P, Lippens S, Vandenabeele P, Declercq W (2009) The emerging roles of serine protease cascades in the epidermis. Trends Biochem Sci 34:453–463CrossRefPubMedGoogle Scholar
  39. Rokyta DR, Lemmon AR, Margres MJ, Aronow K (2012) The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genom 13:312CrossRefGoogle Scholar
  40. Sagisaka A, Fujita K, Nakamura Y, Ishibashi J, Noda H, Imanishi S, Mita K, Yamakawa M, Tanaka H (2010) Genome-wide analysis of host gene expression in the silkworm cells infected with Bombyx mori nucleopolyhedrovirus. Virus Res 147:166–175CrossRefPubMedGoogle Scholar
  41. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shobahah J, Xue S, Hu D, Zhao C, Wei M, Quan Y, Yu W (2017) Quantitative phosphoproteome on the silkworm (Bombyx mori) cells infected with baculovirus. Virol J 14:117CrossRefPubMedPubMedCentralGoogle Scholar
  43. Steen PW, Tian S, Tully SE, Cravatt BF, Lemosy EK (2010) Activation of Snake in a serine protease cascade that defines the dorsoventral axis is atypical and pipe-independent in Drosophila embryos. FEBS Lett 584:3557–3560CrossRefPubMedPubMedCentralGoogle Scholar
  44. Stein D, Nüsslein-Volhard C (1992) Multiple extracellular activities in Drosophila egg perivitelline fluid are required for establishment of embryonic dorsal-ventral polarity. Cell 68:429–440CrossRefPubMedGoogle Scholar
  45. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich AG, Pomeroy SL, Golub TR, Lander ES (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545–15550CrossRefPubMedPubMedCentralGoogle Scholar
  46. van Houte S, Ros VID, Mastenbroek TG, Vendrig NJ, Hoover K, Spitzen J, van Oers MM (2012) Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior. PLoS ONE 7:e46933CrossRefPubMedPubMedCentralGoogle Scholar
  47. van Houte S, Ros VID, van Oers MM (2014) Hyperactivity and tree-top disease induced by the baculovirus AcMNPV in Spodoptera exigua larvae are governed by independent mechanisms. Naturwissenschaften 101:347–350CrossRefPubMedGoogle Scholar
  48. van Houte S, van Oers MM, Han Y, Vlak JM, Ros VID (2015) Baculovirus infection triggers a positive phototactic response in caterpillars: a response to Dobson et al. (2015). Biol Lett 11:20150633CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang G, Zhang J, Shen Y, Zheng Q, Feng M, Xiang X, Wu X (2015) Transcriptome analysis of the brain of the silkworm Bombyx mori infected with Bombyx mori nucleopolyhedrovirus: a new insight into the molecular mechanism of enhanced locomotor activity induced by viral infection. J Invertebr Pathol 128:37–43CrossRefPubMedGoogle Scholar
  50. Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921–926CrossRefPubMedPubMedCentralGoogle Scholar
  51. Xue J, Qiao N, Zhang W, Cheng R-L, Zhang X-Q, Bao Y-Y, Xu Y-P, Gu L-Z, Han J-DJ, Zhang C-X (2012) Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J Virol 86:7345–7359CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Crop Stress Biology for Arid AreasNorthwest A&F UniversityYanglingChina

Personalised recommendations