Molecular characterization of geminivirus-derived small RNAs in different plant species.

Arabidopsis/virology; Arabidopsis Proteins/metabolism; Geminiviridae/genetics; Methylation; Phosphorylation; Plants/virology; RNA Interference; RNA Viruses/genetics; RNA, Small Interfering/chemistry/classification/metabolism; RNA, Viral/chemistry/classification/metabolism; Tobacco/virology

Abstract :

[en] DNA geminiviruses are thought to be targets of RNA silencing. Here, we characterize small interfering (si) RNAs-the hallmarks of silencing-associated with Cabbage leaf curl begomovirus in Arabidopsis and African cassava mosaic begomovirus in Nicotiana benthamiana and cassava. We detected 21, 22 and 24 nt siRNAs of both polarities, derived from both the coding and the intergenic regions of these geminiviruses. Genetic evidence showed that all the 24 nt and a substantial fraction of the 22 nt viral siRNAs are generated by the dicer-like proteins DCL3 and DCL2, respectively. The viral siRNAs were 5' end phosphorylated, as shown by phosphatase treatments, and methylated at the 3'-nucleotide, as shown by HEN1 miRNA methylase-dependent resistance to beta-elimination. Similar modifications were found in all types of endogenous and transgene-derived siRNAs tested, but not in a major fraction of siRNAs from a cytoplasmic RNA tobamovirus. We conclude that several distinct silencing pathways are involved in DNA virus-plant interactions.

Disciplines :

Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Akbergenov, Rashid

Si-Ammour, Azeddine

Blevins, Todd

Amin, Imran

Kutter, Claudia

Vanderschuren, Hervé ; Université de Liège - ULiège > Sciences agronomiques > Biologie végétale

Zhang, Peng

Gruissem, Wilhelm

Meins, Frederick Jr

Hohn, Thomas

Pooggin, Mikhail M.

Language :

English

Title :

Molecular characterization of geminivirus-derived small RNAs in different plant species.

Publication date :

2006

Journal title :

Nucleic Acids Research

ISSN :

0305-1048

eISSN :

1362-4962

Publisher :

Oxford University Press, United Kingdom

Volume :

Issue :

Pages :

462-71

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 06 October 2014

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Scopus citations^®

219

Scopus citations^®
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177

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215

Bibliography

Bartel,D.P. (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
Meins,F.,Jr, Si-Ammour,A. and Blevins,T. (2005) RNA silencing systems and their relevance to plant development. Annu. Rev. Cell Dev. Biol., 21, 297-318.
Baulcombe,D. (2005) RNA silencing. Trends Biochem. Sci., 30, 290-293.
Baumberger,N. and Baulcombe,D.C. (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl Acad. Sci. USA, 102, 11928-11933.
Zilberman,D., Cao,X., Johansen,L.K., Xie,Z., Carrington,J.C. and Jacobsen,S.E. (2004) Role of Arabidopsis ARGONAUTE4 in RNA-directed DNA methylation triggered by inverted repeats. Curr. Biol., 14, 1214-1220.
Voinnet,O. (2005) Induction and suppression of RNA silencing: Insights from viral infections. Nature Rev. Genet., 6, 206-220.
Hamilton,A.J. and Baulcombe,D.C. (1999) A species of small antisense RNA in post-transcriptional gene silencing in plants. Science, 286, 950-952.
Szittya,G., Molnar,A., Silhavy,D., Hornyik,C. and Burgyan,J. (2002) Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell, 14, 359-372.
Kubota,K., Tsuda,S., Tamai,A. and Meshi,T. (2003) Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J. Virol., 77, 11016-11026.
Xie,Z., Johansen,L.K., Gustafson,A.M., Kasschau,K.D., Lellis,A.D., Zilberman,D., Jacobsen,S.E. and Carrington,J.C. (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol., 2, E104.
Molnar,A., Csorba,T., Lakatos,L., Varallyay,E., Lacomme,C. and Burgyan,J. (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J. Virol., 79, 7812-7818.
Lucioli,A., Noris,E., Brunetti,A., Tavazza,R., Ruzza,V., Castillo,A.G., Bejarano,E.R., Accotto,G.P. and Tavazza,M. (2003) Tomato yellow leaf curl Sardinia virus rep-derived resistance to homologous and heterologous geminiviruses occurs by different mechanisms and is overcome if virus-mediated transgene silencing is activated. J. Virol., 77, 6785-6798.
Chellappan,P., Vanitharani,R. and Fauquet,C.M. (2004) Short interfering RNA accumulation correlates with host recovery in DNA virus-infected hosts, and gene silencing targets specific viral sequences. J. Virol., 78, 7465-7477.
Zhang,P., Vanderschuren,H., Fütterer,J. and Gruissem,W. (2005) Resistance to cassava mosaic disease in transgenic cassava expressing antisense RNAs targeting virus replication genes. Plant Biotech. J., 3, 385-397.
Lakatos,L., Szittya,G., Silhavy,D. and Burgyan,J. (2004) Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J., 23, 876-884.
Chellappan,P., Vanitharani,R. and Fauquet,C.M. (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. Proc. Natl Acad. Sci. USA, 102, 10381-10386.
Lecellier,C.H., Dunoyer,P., Arar,K., Lehmann-Che,J., Eyquem,S., Himber,C., Saib,A. and Voinnet,O. (2005) A cellular microRNA mediates antiviral defense in human cells. Science, 308, 557-560.
Elbashir,S.M., Lendeckel,W. and Tuschl,T. (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev., 15, 188-200.
Tang,G., Reinhart,B.J., Bartel,D.P. and Zamore,P.D. (2003) A biochemical framework for RNA silencing in plants. Genes Dev., 17, 49-63.
Schauer,S.E., Jacobsen,S.E., Meinke,D.W. and Ray,A. (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci., 7, 487-491.
Gasciolli,V., Mallory,A.C., Bartel,D.P. and Vaucheret,H. (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol., 15, 1494-1500.
Kurihara,Y. and Watanabe,Y. (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl Acad. Sci. USA, 101, 12753-12758.
Herr,A.J., Jensen,M.B., Dalmay,T. and Baulcombe,D.C. (2005) RNA polymerase IV directs silencing of endogenous DNA. Science, 308, 118-120.
Vazquez,F., Vaucheret,H., Rajagopalan,R., Lepers,C., Gasciolli,V., Mallory,A.C., Hilbert,J.L., Bartel,D.P. and Crete,P. (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell, 16, 69-79.
Allen,E., Xie,Z., Gustafson,A.M. and Carrington,J.C. (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell, 121, 207-221.
Xie,Z., Allen,E., Wilken,A. and Carrington,J.C. (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 102, 12984-1289.
Han,M.H., Goud,S., Song,L. and Fedoroff,N. (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl Acad. Sci. USA, 101, 1093-1098.
Vazquez,F., Gasciolli,V., Crete,P. and Vaucheret,H. (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr. Biol., 14, 346-351.
Hiraguri,A., Itoh,R., Kondo,N., Nomura,Y., Aizawa,D., Murai,Y., Koiwa,H., Seki,M., Shinozaki,K. and Fukuhara,T. (2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol., 57, 173-188.
Park,W., Li,J., Song,R., Messing,J. and Chen,X. (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol., 12, 1484-1495.
Boutet,S., Vazquez,F., Liu,J., Beclin,C., Fagard,M., Gratias,A., Morel,J.B., Crete,P., Chen,X. and Vaucheret,H. (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr. Biol., 13, 843-848.
Yu,B., Yang,Z., Li,J., Minakhina,S., Yang,M., Padgett,R.W., Steward,R. and Chen,X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science, 307, 932-935.
Ebhardt,H.A., Thi,E.P., Wang,M.B. and Unrau,P.J. (2005) Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc. Natl Acad. Sci. USA, 102, 13398-13403.
Li,J., Yang,Z., Yu,B., Liu,J. and Chen,X. (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol., 15, 1501-1507.
Rybicki,E.P., Briddon,R.W., Brown,J.K., Fauquet,C.M., Maxwell,D.P., Harrison,B.D., Markham,P.G., Bisaro,D.M., Robinson,D. and Stanley,J. (2000) Family Geminiviridae. In van Regenmortel,M.H.V., Fauquet,C.M., Bishop,D.H.L. et al. (eds), Virus Taxonomy: Classification and Nomenclature of Viruses. Academic Press, NY, pp. 285-297.
Pilartz,M. and Jeske,H. (2003) Mapping of abutilon mosaic geminivirus minichromosomes. J. Virol., 77, 10808-10818.
Hanley-Bowdoin,L., Settlage,S.B., Orozco,B.M., Nagar,S. and Robertson,D. (1999) Geminiviruses: Models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Plant Sci., 18, 71-106.
Shivaprasad,P.V., Akbergenov,R., Trinks,D., Rajeswaran,R., Veluthambi,K., Hohn,T. and Pooggin,M.M. (2005) Promoters, transcripts, and regulatory proteins of Mungbean yellow mosaic geminivirus. J. Virol., 79, 8149-8163.
Trinks,D., Rajeswaran,R., Shivaprasad,P.V., Akbergenov,R., Oakeley,E.J., Veluthambi,K., Hohn,T. and Pooggin,M.M. (2005) Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J. Virol., 79, 2517-2527.
Stanley,J. and Gay,M.R. (1983) Nucleotide sequence of cassava latent virus DNA. Nature, 301, 260-262.
Hill,J.E., Strandberg,J.O., Hiebert,E. and Lazarowitz,S.G. (1998) Asymmetric infectivity of pseudorecombinants of cabbage leaf curl virus and squash leaf curl virus: Implications for bipartite geminivirus evolution and movement. Virology, 250, 283-292.
Fondong,V.N., Pita,J.S., Rey,M.E., de,Kochko,A., Beachy,R.N. and Fauquet,C.M. (2000) Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon. J. Gen. Virol., 81, 287-297.
Liu,S.J., Bedford,I.D., Briddon,R.W. and Markham,P.G. (1997) Efficient whitefly transmission of African cassava mosaic geminivirus requires sequences from both genomic components. J. Gen. Virol., 78, 1791-1794.
Zhang,P., Legris,G., Coulin,P. and Puonti-Kaerlas,J. (2000) Production of stably transformed cassava plants via particle bombardment. Plant Cell Rep., 19, 939-945.
Turnage,M.A., Muangsan,N., Peele,C.G. and Robertson,D. (2002) Geminivirus-based vectors for gene silencing in Arabidopsis. Plant J., 30, 107-114.
Aguilar,I., Sanchez,F., Martin,Martin,A., Martinez-Herrera,D. and Ponz,F. (1996) Nucleotide sequence of Chinese rape mosaic virus (oilseed rape mosaic virus), a crucifer tobamovirus infectious on Arabidopsis thaliana. Plant Mol. Biol., 30, 191-197.
Pooggin,M., Shivaprasad,P.V., Veluthambi,K. and Hohn,T. (2003) RNAi targeting of DNA virus in plants. Nat. Biotechnol., 21, 131-132.
Goodall,G.J. and Filipowicz,W. (1989) The AU-rich sequences present in the introns of plant nuclear pre-mRNAs are required for splicing. Cell, 58, 473-483.
Zhang,P., Potrykus,I. and Puonti-Kaerlas,J. (2000) Efficient production of transgenic cassava using negative and positive selection. Transgenic Res, 9, 405-415.
Glazov,E., Phillips,K., Budziszewski,G.J., Schob,H., Meins,F.Jr and Levin,J.Z. (2003) A gene encoding an RNase D exonuclease-like protein is required for post-transcriptional silencing in Arabidopsis. Plant J., 35, 342-349.
Shen,B. and Goodman,H.M. (2004) Uridine addition after microRNA-directed cleavage. Science, 306, 997.
Vanitharani,R., Chellappan,P., Pita,J.S. and Fauquet,C.M. (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J. Virol., 78, 9487-9498.
Wang,H., Buckley,K.J., Yang,X., Buchmann,R.C. and Bisaro,D.M. (2005) Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol., 79, 7410-7418.