1887

Journal of General Virology header logo

Volume 86, Issue 9

Specific and common changes in gene expression in response to infection by enveloped viruses Free

Abstract

Microarrays derived from expressed sequence tags were used to test the hypothesis that genetically distinct enveloped viruses elicit unique changes in gene expression. The results of our study, which included (SYNV), a plant rhabdovirus that replicates in the nucleus of infected cells, and (INSV), a plant bunyavirus that replicates in the cytoplasm, were consistent with this hypothesis. Statistically significant changes (⩽0·01) in the expression of 275, 2646 and 4165 genes were detected in response to INSV at 2, 4 and 5 days post-inoculation (d.p.i.), respectively. In contrast, 35, 665 and 1458 genes were expressed differentially in response to SYNV at 5, 11 and 14 d.p.i., respectively. The microarray results were verified by Northern hybridization using a subset of these genes as probes. Notably, INSV, but not SYNV, induced expression of small heat-shock protein genes to high levels. In contrast to SYNV, infection by INSV resulted in downregulation of all histone genes, of which the downregulation of histone 2b expression to very low levels was confirmed by Northern hybridization. The expression of a putative WRKY transcription factor at 11 d.p.i., but not at 5 or 14 d.p.i., in SYNV-infected tissue suggested that the temporal response to virus infection was identified readily using our experimental design. Overall, infection by INSV resulted in larger fold changes in host gene expression relative to infection by SYNV. Taken together, the present data demonstrate differential responses of a common host to two genetically distinct viruses.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.81043-0
2005-09-01
2024-05-05
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/9/vir862615.html?itemId=/content/journal/jgv/10.1099/vir.0.81043-0&mimeType=html&fmt=ahah

References

  1. Ahmed M., Lyles D. S. 1997; Identification of a consensus mutation in M protein of vesicular stomatitis virus from persistently infected cells that affects inhibition of host-directed gene expression. Virology 237:378–388 [CrossRef]
     [Google Scholar]
  2. Aranda M., Maule A. 1998; Virus-induced host gene shutoff in animals and plants. Virology 243:261–267 [CrossRef]
     [Google Scholar]
  3. Aranda M. A., Escaler M., Wang D., Maule A. J. 1996; Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc Natl Acad Sci U S A 93:15289–15293 [CrossRef]
     [Google Scholar]
  4. Bendahmane A., Querci M., Kanyuka K., Baulcombe D. C. 2000; Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. Plant J 21:73–81 [CrossRef]
     [Google Scholar]
  5. Borisjuk N., Borisjuk L., Petjuch G., Hemleben V. 1994; Comparison of nuclear ribosomal RNA genes among Solanum species and other Solanaceae. Genome 37:271–279 [CrossRef]
     [Google Scholar]
  6. D'Arcy W. G. 1979; The classification of the Solanaceae. In The Biology and Taxonomy of the Solanaceae . pp  3–47 Edited by Hawkes J. G., Lester R. N., Skelding A. D. London: Academic Press;
  7. Daughtrey M. L., Jones R. K., Moyer J. W., Daub M. E., Baker J. R. 1997; Tospoviruses strike the greenhouse industry: INSV has become a major pathogen on flower crops. Plant Dis 81:1220–1230 [CrossRef]
     [Google Scholar]
  8. Escobar N. M., Haupt S., Thow G., Boevink P., Chapman S., Oparka K. 2003; High-throughput viral expression of cDNA–green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. Plant Cell 15:1507–1523 [CrossRef]
     [Google Scholar]
  9. Eulgem T., Rushton P. J., Robatzek S., Somssich I. E. 2000; The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206 [CrossRef]
     [Google Scholar]
  10. Golem S., Culver J. N. 2003; Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana . Mol Plant Microbe Interact 16:681–688 [CrossRef]
     [Google Scholar]
  11. Goodin M. M., Dietzgen R. G., Schichnes D., Ruzin S., Jackson A. O. 2002; pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. Plant J 31:375–383 [CrossRef]
     [Google Scholar]
  12. Heaton L. A., Hillman B. I., Hunter B. G., Zuidema D., Jackson A. O. 1989; Physical map of the genome of sonchus yellow net virus, a plant rhabdovirus with six genes and conserved gene junction sequences. Proc Natl Acad Sci U S A 86:8665–8668 [CrossRef]
     [Google Scholar]
  13. Hogenhout S. A., Redinbaugh M. G., Ammar el-D. 2003; Plant and animal rhabdovirus host range: a bug's view. Trends Microbiol 11:264–271 [CrossRef]
     [Google Scholar]
  14. Jackson A. O., Christie S. R. 1977; Purification and some physiochemical properties of sonchus yellow net virus. Virology 77:344–355 [CrossRef]
     [Google Scholar]
  15. Jackson A. O., Francki R. I. B., Zuidema D. 1987; Biology, structure and replication of plant rhabdoviruses. In The Rhabdoviruses pp  427–508 Edited by Wagner R. R. New York: Plenum;
     [Google Scholar]
  16. Jones R. W., Jackson A. O. 1990; Replication of sonchus yellow net virus in infected protoplasts. Virology 179:815–820 [CrossRef]
     [Google Scholar]
  17. Law M. D., Speck J., Moyer J. W. 1992; The M RNA of impatiens necrotic spot Tospovirus (Bunyaviridae) has an ambisense genomic organization. Virology 188:732–741 [CrossRef]
     [Google Scholar]
  18. Lewis S. E. 2005; Gene Ontology: looking backwards and forwards. Genome Biol 6:103 [CrossRef]
     [Google Scholar]
  19. Liu Y., Burch-Smith T., Schiff M., Feng S., Dinesh-Kumar S. P. 2004; Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279:2101–2108 [CrossRef]
     [Google Scholar]
  20. Lu R., Malcuit I., Moffett P. 7 other authors 2003; High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22:5690–5699 [CrossRef]
     [Google Scholar]
  21. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  22. Marathe R., Guan Z., Anandalakshmi R., Zhao H., Dinesh-Kumar S. 2004; Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol 55:501–520 [CrossRef]
     [Google Scholar]
  23. Martin D., Brun C., Remy E., Mouren P., Thieffry D., Jacq B. 2004; GOToolBox: functional analysis of gene datasets based on gene ontology. Genome Biol 5:R101 [CrossRef]
     [Google Scholar]
  24. Martins C. R. F., Johnson J. A., Lawrence D. M. 8 other authors 1998; Sonchus yellow net rhabdovirus nuclear viroplasms contain polymerase-associated proteins. J Virol 72:5669–5679
     [Google Scholar]
  25. Maule A., Leh V., Lederer C. 2002; The dialogue between viruses and hosts in compatible interactions. Curr Opin Plant Biol 5:279–284 [CrossRef]
     [Google Scholar]
  26. Qanungo K. R., Shaji D., Mathur M., Banerjee A. K. 2004; Two RNA polymerase complexes from vesicular stomatitis virus-infected cells that carry out transcription and replication of genome RNA. Proc Natl Acad Sci U S A 101:5952–5957 [CrossRef]
     [Google Scholar]
  27. Ronning C. M., Stegalkina S. S., Ascenzi R. A. 24 other authors 2003; Comparative analyses of potato expressed sequence tag libraries. Plant Physiol 131:419–429 [CrossRef]
     [Google Scholar]
  28. van Poelwijk F., Kolkman J., Goldbach R. 1996; Sequence analysis of the 5′ ends of tomato spotted wilt virus N mRNAs. Arch Virol 141:177–184 [CrossRef]
     [Google Scholar]
  29. Weck P. K., Wagner R. R. 1978; Inhibition of RNA synthesis in mouse myeloma cells infected with vesicular stomatitis virus. J Virol 25:770–780
     [Google Scholar]
  30. Whitham S. A., Quan S., Chang H.-S., Cooper B., Estes B., Zhu T., Wang X., Hou Y.-M. 2003; Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33:271–283 [CrossRef]
     [Google Scholar]
  31. Zhirnov O. P., Konakova T. E., Garten W., Klenk H.-D. 1999; Caspase-dependent N-terminal cleavage of influenza virus nucleocapsid protein in infected cells. J Virol 73:10158–10163
     [Google Scholar]
  32. Zhong G. V., Burns J. K. 2003; Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53:117–131 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.81043-0
Loading
Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped viruses
J. Gen. Virol. 86, 2615 (2005); https://doi.org/10.1099/vir.0.81043-0
/content/journal/jgv/10.1099/vir.0.81043-0
/content/journal/jgv/10.1099/vir.0.81043-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error