Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
American Association for Cancer Research

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Originally published in Science Express on 1 June 2006
Science 7 July 2006:
Vol. 313. no. 5783, pp. 68 - 71
DOI: 10.1126/science.1128214

Research Articles

Hierarchical Action and Inhibition of Plant Dicer-Like Proteins in Antiviral Defense

Angélique Deleris,1 Javier Gallego-Bartolome,1 Jinsong Bao,2 Kristin D. Kasschau,2 James C. Carrington,2 Olivier Voinnet1*

The mechanisms underlying induction and suppression of RNA silencing in the ongoing plant-virus arms race are poorly understood. We show here that virus-derived small RNAs produced by Arabidopsis Dicer-like 4 (DCL4) program an effector complex conferring antiviral immunity. Inhibition of DCL4 by a viral-encoded suppressor revealed the subordinate antiviral activity of DCL2. Accordingly, inactivating both DCL2 and DCL4 was necessary and sufficient to restore systemic infection of a suppressor-deficient virus. The effects of DCL2 were overcome by increasing viral dosage in inoculated leaves, but this could not surmount additional, non–cell autonomous effects of DCL4 specifically preventing viral unloading from the vasculature. These findings define a molecular framework for studying antiviral silencing and defense in plants.

1 Institut de Biologie Moléculaire des Plantes, CNRS Unité Propre de Recherche (UPR) 2357, 12, rue du Général Zimmer, 67084 Strasbourg Cedex, France.
2 Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331, USA.

* To whom correspondence should be addressed. E-mail: olivier.voinnet{at}ibmp-ulp.u-strasbg.fr

Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Conifers have a unique small RNA silencing signature.
E. V. Dolgosheina, R. D. Morin, G. Aksay, S. C. Sahinalp, V. Magrini, E. R. Mardis, J. Mattsson, and P. J. Unrau (2008)
RNA 14, 1508-1515
   Abstract »    Full Text »    PDF »
From the Cover: The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1.
Z. Dong, M.-H. Han, and N. Fedoroff (2008)
PNAS 105, 9970-9975
   Abstract »    Full Text »    PDF »
Inhibition of 3' modification of small RNAs in virus-infected plants require spatial and temporal co-expression of small RNAs and viral silencing-suppressor proteins.
R. Lozsa, T. Csorba, L. Lakatos, and J. Burgyan (2008)
Nucleic Acids Res. 36, 4099-4107
   Abstract »    Full Text »    PDF »
Effects of viral silencing suppressors on tobacco ringspot virus infection in two Nicotiana species.
S. A. Siddiqui, C. Sarmiento, M. Kiisma, S. Koivumaki, A. Lemmetty, E. Truve, and K. Lehto (2008)
J. Gen. Virol. 89, 1502-1508
   Abstract »    Full Text »    PDF »
Structural and Genetic Requirements for the Biogenesis of Tobacco Rattle Virus-Derived Small Interfering RNAs.
L. Donaire, D. Barajas, B. Martinez-Garcia, L. Martinez-Priego, I. Pagan, and C. Llave (2008)
J. Virol. 82, 5167-5177
   Abstract »    Full Text »    PDF »
Hairpin RNAs derived from RNA polymerase II and polymerase III promoter-directed transgenes are processed differently in plants.
M.-B. Wang, C. A. Helliwell, L.-M. Wu, P. M. Waterhouse, W. J. Peacock, and E. S. Dennis (2008)
RNA 14, 903-913
   Abstract »    Full Text »    PDF »
Activity Range of Arabidopsis Small RNAs Derived from Different Biogenesis Pathways.
E. M. Tretter, J. P. Alvarez, Y. Eshed, and J. L. Bowman (2008)
Plant Physiology 147, 58-62
   Full Text »    PDF »
RNAs as extracellular signaling molecules.
M. E Dinger, T. R Mercer, and J. S Mattick (2008)
J. Mol. Endocrinol. 40, 151-159
   Abstract »    Full Text »    PDF »
Characterization of Hypovirus-Derived Small RNAs Generated in the Chestnut Blight Fungus by an Inducible DCL-2-Dependent Pathway.
X. Zhang, G. C. Segers, Q. Sun, F. Deng, and D. L. Nuss (2008)
J. Virol. 82, 2613-2619
   Abstract »    Full Text »    PDF »
Protease Activity, Self Interaction, and Small Interfering RNA Binding of the Silencing Suppressor P1b from Cucumber Vein Yellowing Ipomovirus.
A. Valli, G. Dujovny, and J. A. Garcia (2008)
J. Virol. 82, 974-986
   Abstract »    Full Text »    PDF »
Specific Enrichment of miRNAs in Arabidopsis thaliana Infected with Tobacco mosaic virus.
Y. Tagami, N. Inaba, N. Kutsuna, Y. Kurihara, and Y. Watanabe (2007)
DNA Res
   Abstract »    Full Text »    PDF »
Heterologous Expression of Viral RNA Interference Suppressors: RISC Management.
H. B. Scholthof (2007)
Plant Physiology 145, 1110-1117
   Full Text »    PDF »
Recovery of Nicotiana benthamiana Plants from a Necrotic Response Induced by a Nepovirus Is Associated with RNA Silencing but Not with Reduced Virus Titer.
J. Jovel, M. Walker, and H. Sanfacon (2007)
J. Virol. 81, 12285-12297
   Abstract »    Full Text »    PDF »
A cucumber mosaic virus mutant lacking the 2b counter-defence protein gene provides protection against wild-type strains.
H. Ziebell, T. Payne, J. O. Berry, J. A. Walsh, and J. P. Carr (2007)
J. Gen. Virol. 88, 2862-2871
   Abstract »    Full Text »    PDF »
Modification of Small RNAs Associated with Suppression of RNA Silencing by Tobamovirus Replicase Protein.
H. Vogler, R. Akbergenov, P. V. Shivaprasad, V. Dang, M. Fasler, M.-O. Kwon, S. Zhanybekova, T. Hohn, and M. Heinlein (2007)
J. Virol. 81, 10379-10388
   Abstract »    Full Text »    PDF »
Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis.
C. A. Brosnan, N. Mitter, M. Christie, N. A. Smith, P. M. Waterhouse, and B. J. Carroll (2007)
PNAS 104, 14741-14746
   Abstract »    Full Text »    PDF »
DCL4 Targets Cucumber Mosaic Virus Satellite RNA at Novel Secondary Structures.
Q.-S. Du, C.-G. Duan, Z.-H. Zhang, Y.-Y. Fang, R.-X. Fang, Q. Xie, and H.-S. Guo (2007)
J. Virol. 81, 9142-9151
   Abstract »    Full Text »    PDF »
A Cluster of Disease Resistance Genes in Arabidopsis Is Coordinately Regulated by Transcriptional Activation and RNA Silencing.
H. Yi and E. J. Richards (2007)
PLANT CELL 19, 2929-2939
   Abstract »    Full Text »    PDF »
Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins.
G. Moissiard, E. A. Parizotto, C. Himber, and O. Voinnet (2007)
RNA 13, 1268-1278
   Abstract »    Full Text »    PDF »
Artificial MicroRNA-Mediated Virus Resistance in Plants.
J. Qu, J. Ye, and R. Fang (2007)
J. Virol. 81, 6690-6699
   Abstract »    Full Text »    PDF »
DICER-LIKE 1 and DICER-LIKE 3 Redundantly Act to Promote Flowering via Repression of FLOWERING LOCUS C in Arabidopsis thaliana.
R. J. Schmitz, L. Hong, K. E. Fitzpatrick, and R. M. Amasino (2007)
Genetics 176, 1359-1362
   Abstract »    Full Text »    PDF »
Suppression of Antiviral Silencing by Cucumber Mosaic Virus 2b Protein in Arabidopsis Is Associated with Drastically Reduced Accumulation of Three Classes of Viral Small Interfering RNAs.
J. A. Diaz-Pendon, F. Li, W.-X. Li, and S.-W. Ding (2007)
PLANT CELL 19, 2053-2063
   Abstract »    Full Text »    PDF »
Molecular Bases of Viral RNA Targeting by Viral Small Interfering RNA-Programmed RISC.
V. Pantaleo, G. Szittya, and J. Burgyan (2007)
J. Virol. 81, 3797-3806
   Abstract »    Full Text »    PDF »
A Structured Viroid RNA Serves as a Substrate for Dicer-Like Cleavage To Produce Biologically Active Small RNAs but Is Resistant to RNA-Induced Silencing Complex-Mediated Degradation.
A. Itaya, X. Zhong, R. Bundschuh, Y. Qi, Y. Wang, R. Takeda, A. R. Harris, C. Molina, R. S. Nelson, and B. Ding (2007)
J. Virol. 81, 2980-2994
   Abstract »    Full Text »    PDF »
Role of RNA polymerase IV in plant small RNA metabolism.
X. Zhang, I. R. Henderson, C. Lu, P. J. Green, and S. E. Jacobsen (2007)
PNAS 104, 4536-4541
   Abstract »    Full Text »    PDF »
Genome-Wide Analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 Pathway in Arabidopsis Reveals Dependency on miRNA- and tasiRNA-Directed Targeting.
M. D. Howell, N. Fahlgren, E. J. Chapman, J. S. Cumbie, C. M. Sullivan, S. A. Givan, K. D. Kasschau, and J. C. Carrington (2007)
PLANT CELL 19, 926-942
   Abstract »    Full Text »    PDF »
Tomato Chlorotic Mottle Virus Is a Target of RNA Silencing but the Presence of Specific Short Interfering RNAs Does Not Guarantee Resistance in Transgenic Plants.
S. G. Ribeiro, H. Lohuis, R. Goldbach, and M. Prins (2007)
J. Virol. 81, 1563-1573
   Abstract »    Full Text »    PDF »
RNAi-associated ssRNA-specific ribonucleases in Tombusvirus P19 mutant-infected plants and evidence for a discrete siRNA-containing effector complex.
R. T. Omarov, J. J. Ciomperlik, and H. B. Scholthof (2007)
PNAS 104, 1714-1719
   Abstract »    Full Text »    PDF »
RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis Dicer-like proteins.
G. Moissiard and O. Voinnet (2006)
PNAS 103, 19593-19598
   Abstract »    Full Text »    PDF »
Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing.
T. Blevins, R. Rajeswaran, P. V. Shivaprasad, D. Beknazariants, A. Si-Ammour, H.-S. Park, F. Vazquez, D. Robertson, F. Meins Jr, T. Hohn, et al. (2006)
Nucleic Acids Res. 34, 6233-6246
   Abstract »    Full Text »    PDF »
Induction of Gene Silencing by Hairpin RNA Expression in Tetrahymena thermophila Reveals a Second Small RNA Pathway.
R. A. Howard-Till and M.-C. Yao (2006)
Mol. Cell. Biol. 26, 8731-8742
   Abstract »    Full Text »    PDF »
The blossoming of RNA biology: Novel insights from plant systems.
J. Bove, C. L.H. Hord, and M. A. Mullen (2006)
RNA 12, 2035-2046
   Full Text »    PDF »
Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense.
X. Zhang, Y.-R. Yuan, Y. Pei, S.-S. Lin, T. Tuschl, D. J. Patel, and N.-H. Chua (2006)
Genes & Dev. 20, 3255-3268
   Abstract »    Full Text »    PDF »
The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster..
R. P. van Rij, M.-C. Saleh, B. Berry, C. Foo, A. Houk, C. Antoniewski, and R. Andino (2006)
Genes & Dev. 20, 2985-2995
   Abstract »    Full Text »    PDF »



ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)