Transcriptome and small RNAome profiling uncovers how a recombinant begomovirus evades RDRγ-mediated silencing of viral genes and outcompetes its parental virus in mixed infection

Tomato yellow leaf curl virus (TYLCV, genus Begomovirus , family Geminiviridae ) causes severe disease of cultivated tomatoes. Geminiviruses replicate circular single-stranded genomic DNA via rolling-circle and recombination-dependent mechanisms, frequently generating recombinants in mixed infection...

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Vydáno v:PLoS pathogens Ročník 20; číslo 1; s. e1011941
Hlavní autoři: Jammes, Margaux, Golyaev, Victor, Fuentes, Alejandro, Laboureau, Nathalie, Urbino, Cica, Plissonneau, Clemence, Peterschmitt, Michel, Pooggin, Mikhail M.
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Public Library of Science 01.01.2024
Public Library of Science (PLoS)
Témata:
Biochemistry, Molecular Biology
Biology and life sciences
Coat protein
Cultivars
Cultivation
Deoxyribonucleic acid
Disease resistance
DNA
DNA methylation
DNA-directed RNA polymerase
Fruit cultivation
Gene silencing
Genes
Genomes
Genomics
Infections
Intermediates
Leaf-curl
Life Sciences
Mixed infection
Phytopathology and phytopharmacy
Plant diseases
Plant resistance
Plant virus diseases
Plant viruses
Post-transcription
Proteins
Recombinants
Recombination
Replication
Replication origins
Ribonucleic acid
RNA
RNA polymerase
RNA-directed RNA polymerase
Single-stranded DNA
siRNA
Tomatoes
Transcriptomes
Vegetal Biology
Viruses
Yellow leaf
Morocco
ISSN:1553-7374, 1553-7366, 1553-7374
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Shrnutí:Tomato yellow leaf curl virus (TYLCV, genus Begomovirus , family Geminiviridae ) causes severe disease of cultivated tomatoes. Geminiviruses replicate circular single-stranded genomic DNA via rolling-circle and recombination-dependent mechanisms, frequently generating recombinants in mixed infections. Circular double-stranded intermediates of replication also serve as templates for Pol II bidirectional transcription. IS76, a recombinant derivative of TYLCV with a short sequence in the bidirectional promoter/origin-of-replication region acquired from a related begomovirus, outcompetes TYLCV in mixed infection and breaks disease resistance in tomato Ty-1 cultivars. Ty-1 encodes a γ-clade RNA-dependent RNA polymerase (RDRγ) implicated in Dicer-like (DCL)-mediated biogenesis of small interfering (si)RNAs directing gene silencing. Here, we profiled transcriptome and small RNAome of Ty-1 resistant and control susceptible plants infected with TYLCV, IS76 or their combination at early and late infection stages. We found that RDRγ boosts production rates of 21, 22 and 24 nt siRNAs from entire genomes of both viruses and modulates DCL activities in favour of 22 and 24 nt siRNAs. Compared to parental TYLCV, IS76 undergoes faster transition to the infection stage favouring rightward transcription of silencing suppressor and coat protein genes, thereby evading RDRγ activity and facilitating its DNA accumulation in both single and mixed infections. In coinfected Ty-1 plants, IS76 efficiently competes for host replication and transcription machineries, thereby impairing TYLCV replication and transcription and forcing its elimination associated with further increased siRNA production. RDRγ is constitutively overexpressed in Ty-1 plants, which correlates with begomovirus resistance, while siRNA-generating DCLs (DCL2b/d, DCL3, DCL4) and genes implicated in siRNA amplification (α-clade RDR1) and function (Argonaute2) are upregulated to similar levels in TYLCV- and IS76-infected susceptible plants. Collectively, IS76 recombination facilitates replication and promotes expression of silencing suppressor and coat proteins, which allows the recombinant virus to evade the negative impact of RDRγ-boosted production of viral siRNAs directing transcriptional and posttranscriptional silencing.
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The authors declare no competing interests.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1011941