Dept. of Biological Sciences

Vicki Vance

Professor of Biological Sciences
Ph.D., 1983, Washington University
803-777-3179
vance@biol.sc.edu

The Vance Lab

RNA Silencing: Defense and Counterdefense

Dr. Vance's research is directed toward understanding the molecular basis of plant defense against viruses. The model system currently used in the lab is the synergistic disease caused by a mixed infection of tobacco with potato virus X (PVX) and any of a number of related viruses belonging to the genus Potyvirus, for example tobacco etch virus (TEV). Plants infected singly with either PVX or TEV show low levels of disease symptoms. However, in combination, the two viruses cause a devastating disease, and the dramatic increase in host symptoms is correlated with a large increase in the accumulation of PVX in the infected tissues, but no corresponding increase or decrease in the level of TEV. Such synergistic diseases are common in plants and frequently involve a member of the Potyvirus genus as one of the members of the synergistic pair. Our work with the PVX/potyviral interaction has shown that the synergistic increase in PVX accumulation and the correlated increase in host symptoms does not require replication of the potyvirus, but is mediated by expression of a single potyvirus gene product, the helper-component proteinase (HC-Pro) (see Vance et al, 1995). We further found that expression of HC-Pro in transgenic plants allowed a broad range of unrelated viruses to accumulate to a higher level (see Pruss et al., 1997). This led us to hypthesize that HC-Pro worked by interfering with a general anti-viral defense pathway. We proposed at that time that the anti-viral pathway suppressed by HC-Pro was RNA silencing.

RNA silencing is a remarkable type of gene regulation based on sequence-specific targeting and degradation of RNA. The term refers to related pathways found in organisms as diverse as fungi (quelling), plants (post-transcriptional gene silencing, PTGS), protozoans,and a variety of animals including C. elegans, Drosophila, and mice (RNA interference, RNAi). In these organisms, the process is characterized by conserved genes and biochemical features. One key conserved feature is that the induction of RNA silencing involves dsRNA. In plants, RNA silencing may have evolved as a defense against viruses, many of which replicate via dsRNA intermediates. An intriguing aspect of RNA silencing is that it may be triggered locally and then spread throughout the organism via a mobile silencing signal. The identity of the mobile signal remains unknown, but it is thought to incorporate a nucleic acid component to account for the sequence specificity of the process. Another interesting feature of silencing is the accumulation of small RNAs (called siRNAs) that incorporate into the silencing complex and act as guide RNAs to to target specific molecules for destruction.

Our work with viral synergism and HC-Pro is consistent with the idea that RNA silencing is an anti-viral defense. In recent work we have used HC-Pro as a tool to understand the mechanism of gene silencing. We show that HC-Pro suppresses several classes of RNA silencing. In the case of silencing induced by a single copy sense transgene, we established that HC-Pro acts downstream of the mobile silencing signal and interferes with the accumulation of the small RNAs (see Mallory et al., 2001). We have identified several cellular proteins that interact with HC-Pro in the yeast two-hybrid system. Studies of the role of these proteins in RNA silencing are providing clues about the mechanism and regulation of the silencing pathway. One HC-Pro-interacting protein is a calmodulin-related protein called rgs-CaM, that also suppresses RNA silencing when over-expressed in plants(see Anandalakshmi et al., 2000). The emerging view is that RNA silencing is part of a sophisticated network of interconnected pathways for cellular defense, RNA-surveillance,and development, and may become a powerful tool to experimentally manipulate gene expression (see Vance and Vaucheret, 2001).

Selected Publications:

Mlotshwa, S., Pruss, G. J. and Vance, V. (2008) Small RNAs in Viral Infection and Host Defense, Trends in Plant Science (in press - Epub ahead of print June 10, 2008)

Mlotshwa, S., Pruss, G. J., Peragine, A., Endres. M.W., Li J., Chen, X., Poethig, S., Bowman, L.H. and Vance, V. (2008) DICER-LIKE2 Plays a Primary Role in Transitive Silencing of Transgenes in Arabidopsis. PLoS ONE 3, e1755.

Johnson, C., Bowman, L., Adai, A.T., Vance, V. and Sundaresan, V. (2007) CSRDB: A Small RNA Integrated Database and Browser Resource for Cereals. Nucleic Acids Res. (Database issue), D829-33. Epub 2006 Dec 14.

Mlotshwa, S., Schauer, S., Smith, T. H., Mallory, A., Herr, J.M., Roth, B., Merchant, D., Ray, A., Bowman, L. and Vance, V. (2005) Ectopic DICER-LIKE1 Expression in P1/HC-Pro Arabidopsis Rescues Phenotypic Anomalies but not Defects in MicroRNA and Silencing Pathways. Plant Cell 17, 2873-85.

Adai, A., Johnson, C., Mlotshwa, S., Archer-Evans, S., Manocha, V., Vance, V. and Sundaresan, V. (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res. 15, 78-91.

Roth, B.M., Pruss, G.J. and Vance V.B. (2004) Plant viral suppressors of RNA silencing. Virus Res. 102, 97- 108.

Pruss, G.J., Lawrence, C.B., Bass, T., Li, Q., Bowman, L.H., and Vance, V. (2004) The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology 320, 107-20.

Wang M.B., Bian X.Y., Wu L.M., Liu L.X., Smith N.A., Isenegger D., Wu R.M., Masuta C., Vance V.B., Watson J.M., Rezaian A., Dennis E.S., Waterhouse P.M. (2004) On the role of RNA silencing in the pathogenicity and evolution of viroids and viral satellites. Proc Natl Acad Sci U S A. 101, 3275-80.

Mallory, A.C., Mlotshwa, S., Bowman, L.H. and Vance, V.B. (2003) The capacity of transgenic tobacco to send a systemic RNA silencing signal depends on the nature of the inducing transgene locus. Plant J. 35, 82-92.

Mallory AC, Reinhart BJ, Bartel D, Vance VB, Bowman LH. (2002) A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc Natl Acad Sci U S A. 99, 15228-15233.

Mlotshwa S, Voinnet O, Mette MF, Matzke M, Vaucheret H, Ding SW, Pruss G, Vance VB.(2002) RNA silencing and the mobile silencing signal. Plant Cell 14 Suppl., S289-301.

Mallory AC, Parks G, Endres MW, Baulcombe D, Bowman LH, Pruss GJ, Vance VB. (2002) The amplicon-plus system for high-level expression of transgenes in plants.  Nat Biotechnol. 20, 622-625.

Vance V, Vaucheret H (2001). RNA silencing in plants--defense and counterdefense. Science 292, 2277-80.

Mallory AC, Ely L, Smith TH, Marathe R, Anandalakshmi R, Fagard M, Vaucheret H, Pruss G, Bowman L,Vance VB (2001). HC-Pro Suppression of Transgene Silencing Eliminates the Small RNAs but Not Transgene Methylation or the Mobile Signal. Plant Cell 13, 571-83.

Matzke MA, Matzke AJ, Pruss GJ, Vance VB (2001). RNA-based silencing strategies in plants. Curr Opin Genet Dev. 11, 221-7.

Anandalakshmi, R., Marathe, R., Ge X., Herr, J.M., Mallory, A., Mau, C., Pruss, G., Bowman, L., and Vance, V.B. (2000) A calmodulin-related protein from tobacco suppresses post-transcriptional gene silencing. Science 290, 142-4.

Marathe, R., Anandalakshmi, R., Smith, T., Pruss, G., Vance, V.B. (2000) RNA viruses as inducers, suppressors and targets of post-transcriptional gene silencing. Plant Mol. Biol. 43, 295-306.

Marathe R, Smith TH, Anandalakshmi R, Bowman LH, Fagard M, Mourrain P, Vaucheret H, and Vance VB (2000) Plant viral suppressors of post-transcriptional silencing do not suppress transcriptional silencing. Plant J. 22, 51-59.

Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci USA 1998 Oct 27;95(22):13079-84.

Pruss, G., Ge, X., Shi, X.M., Carrington, J.C., and Vance, V.B. (1997) Plant viral synergism: The potyviral genome encodes a broad range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9, 859-868.

Shi, X.M., Miller, H., Verchot, J., Carrington, J.C. and Vance, V.B. (1997) Mutations in the helper component proteinase (HC-Pro) coding region eliminate potato virus X/potyviral synergism. Virology 231, 35-42.

Sriskanda, V.S., Pruss, G., Ge, X. And Vance, V.B. (1996) An eight nucleotide sequence in the potato virus X 3' untranslated region is required for both host protein binding and viral multiplication. Journal of Virology 70, 5266-5271.

Vance, V.B., Berger, P.H., Carrington, J.C., Hunt, A.G., and Shi, X.M. (1995) 5' proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology 206, 583-590.

Bachman, E., Scott, S., Ge, X. And Vance, V.B. (1994) Complete nucleotide sequence of prune dwarf viral RNA 3: Implications for coat protein activation of genome replication in ilarviruses. Virology 201, 127-131.

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