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PMID: 15220420 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Short interfering RNA accumulation correlates with host recovery in DNA virus-infected hosts, and gene silencing targets specific viral sequences.

Journal of virology ·Vol. 78 ·No. 14 ·2004-07-00 ·Pages 7465-77

Chellappan P, Vanitharani R, Pita J, Fauquet CM

Abstract

Viruses are both inducers and targets of posttranscriptional gene silencing (PTGS), a natural defense mechanism in plants. Here we report molecular evidence of the ability of single-stranded DNA (ssDNA) viruses to induce PTGS in infected plants irrespective of the severity of or recovery from the symptoms. Our results reveal that five distinct species of cassava-infecting geminiviruses were capable of triggering PTGS by producing two classes of virus-specific short interfering RNAs (siRNAs) of 21 to 26 nucleotides in two plant hosts, tobacco (Nicotiana benthamiana) and cassava (Manihot esculenta, Crantz). However, the efficacy of virus-induced PTGS varied depending on the intrinsic features of the virus and its interaction with the plant host. We found that symptom recovery over time in plants infected with the isolates of African cassava mosaic virus (ACMV-[CM]) or Sri Lankan cassava mosaic virus was associated with a much higher level of virus-derived siRNA accumulation compared to plants infected with viruses that do not show symptom recovery. Furthermore, we determined that the C terminus of AC1 that overlaps with the N terminus of AC2 early viral genes involved in virus replication were the primary targets for ACMV-[CM]-induced PTGS, whereas the C terminus of BC1 was targeted for the East African cassava mosaic Cameroon virus. In addition, our results reveal the possibility for double-stranded RNA formation during transcription in ssDNA viruses, which explains in part how these viruses can trigger PTGS in plants.

MeSH Terms
Base Sequence DNA Viruses/genetics,metabolism,physiology Geminiviridae/genetics Gene Expression Regulation, Viral Manihot/virology Molecular Sequence Data Plant Diseases/virology Plant Leaves/virology RNA Interference RNA, Small Interfering/metabolism Tobacco/virology Viral Proteins/genetics,metabolism
Chemicals
RNA, Small Interfering Viral Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chellappan Padmanabhan
International Laboratory for Tropical Agricultural Biotechnology, Danforth Plant Science Center, St Louis, MO 63132, USA.
Vanitharani Ramachandran
Pita Justin
Fauquet Claude M
References (40)
40 references, click to expand
  1. Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression.
    Mol Plant Microbe Interact. 2002 Mar;15(3):203-8 PMID: 11952122
  2. Major polyadenylated transcripts of cassava latent virus and location of the gene encoding coat protein.
    EMBO J. 1985 Jan;4(1):33-7 PMID: 15918226
  3. Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation.
    Crit Rev Biochem Mol Biol. 2000;35(2):105-40 PMID: 10821479
  4. Gene silencing as an adaptive defence against viruses.
    Nature. 2001 Jun 14;411(6839):834-42 PMID: 11459066
  5. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells.
    Nature. 2000 Mar 16;404(6775):293-6 PMID: 10749213
  6. A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing.
    Cell. 1998 Nov 13;95(4):461-70 PMID: 9827799
  7. A similarity between viral defense and gene silencing in plants.
    Science. 1997 Jun 6;276(5318):1558-60 PMID: 18610513
  8. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals.
    Cell. 2000 Mar 31;101(1):25-33 PMID: 10778853
  9. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans.
    Plant Cell. 1990 Apr;2(4):279-289 PMID: 12354959
  10. A biochemical framework for RNA silencing in plants.
    Genes Dev. 2003 Jan 1;17(1):49-63 PMID: 12514099
  11. Post-transcriptional gene silencing by double-stranded RNA.
    Nat Rev Genet. 2001 Feb;2(2):110-9 PMID: 11253050
  12. Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa.
    Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10233-8 PMID: 9294193
  13. Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus.
    Plant Cell. 2002 Feb;14(2):359-72 PMID: 11884680
  14. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells.
    Nature. 2001 May 24;411(6836):494-8 PMID: 11373684
  15. A viral suppressor of gene silencing in plants.
    Proc Natl Acad Sci U S A. 1998 Oct 27;95(22):13079-84 PMID: 9789044
  16. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction.
    Dev Cell. 2003 Feb;4(2):205-17 PMID: 12586064
  17. RNA silencing in plants--defense and counterdefense.
    Science. 2001 Jun 22;292(5525):2277-80 PMID: 11423650
  18. Transcriptional and posttranscriptional plant gene silencing in response to a pathogen
    Science. 1998 Mar 27;279(5359):2113-5 PMID: 9516113
  19. Short interfering RNA-mediated interference of gene expression and viral DNA accumulation in cultured plant cells.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9632-6 PMID: 12886005
  20. 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. 2002 Nov 12;99(23):15228-33 PMID: 12403829
  21. On the role of RNA amplification in dsRNA-triggered gene silencing.
    Cell. 2001 Nov 16;107(4):465-76 PMID: 11719187
  22. The geminivirus BL1 movement protein is associated with endoplasmic reticulum-derived tubules in developing phloem cells.
    J Virol. 1997 May;71(5):3726-33 PMID: 9094647
  23. Identification of tomato golden mosaic virus-specific RNAs in infected plants.
    Virology. 1989 May;170(1):243-50 PMID: 2541538
  24. Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription.
    Plant Cell. 1992 Oct;4(10):1321-31 PMID: 1446172
  25. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13959-64 PMID: 9811908
  26. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14147-52 PMID: 10570213
  27. Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses.
    Plant Cell. 1997 Jun;9(6):859-68 PMID: 9212462
  28. 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. 2003 Jun;77(12):6785-98 PMID: 12767999
  29. RNA silencing as a plant immune system against viruses.
    Trends Genet. 2001 Aug;17(8):449-59 PMID: 11485817
  30. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway.
    Science. 2003 Sep 26;301(5641):1921-5 PMID: 14512631
  31. Evidence of synergism between African cassava mosaic virus and a new double-recombinant geminivirus infecting cassava in Cameroon.
    J Gen Virol. 2000 Jan;81(Pt 1):287-97 PMID: 10640569
  32. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus.
    Cell. 2000 May 26;101(5):543-53 PMID: 10850496
  33. Two classes of short interfering RNA in RNA silencing.
    EMBO J. 2002 Sep 2;21(17):4671-9 PMID: 12198169
  34. A species of small antisense RNA in posttranscriptional gene silencing in plants.
    Science. 1999 Oct 29;286(5441):950-2 PMID: 10542148
  35. Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions.
    EMBO J. 1997 Aug 1;16(15):4738-45 PMID: 9303318
  36. Gene silencing without DNA. rna-mediated cross-protection between viruses
    Plant Cell. 1999 Jul;11(7):1207-16 PMID: 10402423
  37. Role for a bidentate ribonuclease in the initiation step of RNA interference.
    Nature. 2001 Jan 18;409(6818):363-6 PMID: 11201747
  38. Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda.
    J Gen Virol. 2001 Mar;82(Pt 3):655-65 PMID: 11172108
  39. Contribution of the zinc finger to zinc and DNA binding by a suppressor of posttranscriptional gene silencing.
    J Virol. 2003 Jan;77(1):696-700 PMID: 12477872
  40. RNA as a target and an initiator of post-transcriptional gene silencing in transgenic plants.
    Plant Mol Biol. 1996 Oct;32(1-2):79-88 PMID: 8980475
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2004-07-00
Pages
7465-77
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC434130
Subset
IM
Corrections
ErratumIn
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