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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

Jammes Margaux, Golyaev Victor, Fuentes Alejandro, Laboureau Nathalie, Urbino Cica, Plissonneau Clémence, Peterschmitt Michel, Pooggin Mikhail. 2024. 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. PLoS Pathogens, 20 (1):e1011941, 37 p.

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Url - jeu de données - Entrepôt autre : https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA1016149 / Url - jeu de données - Entrepôt autre : https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA1018203 / Url - jeu de données - Entrepôt autre : https://figshare.com/articles/journal_contribution/Supplementary_Methods_Results_and_Discussion_for_S2_Fig_/24992471

Résumé : 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.

Mots-clés Agrovoc : géminivirus enroulement jaune tomat, Geminiviridae, begomovirus, Solanum lycopersicum, virus des végétaux, recombinaison, résistance aux maladies, phylogénie, amélioration des plantes, transcription d'ADN, Transcription génique, génome

Mots-clés géographiques Agrovoc : France, Maroc

Mots-clés libres : Small interfering RNA, Messenger RNA, DNA transcription, Viral replication, Tomatoes, Viral genomics, Viral genome, DNA replication

Agences de financement hors UE : Agence Nationale de la Recherche

Projets sur financement : (FRA) Prévention et contrôle de géminivirus nouveaux et invasifs infectant les cultures légumineuses dans le bassin méditerranéen, Non spécifié

Auteurs et affiliations

  • Jammes Margaux, CIRAD-BIOS-UMR PHIM (FRA)
  • Golyaev Victor, Université de Montpellier (FRA)
  • Fuentes Alejandro, Center for Genetic Engineering and Biotechnology (CUB)
  • Laboureau Nathalie, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0002-0105-3919
  • Urbino Cica, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0002-6215-9389
  • Plissonneau Clémence, Gautier semence (FRA)
  • Peterschmitt Michel, CIRAD-BIOS-UMR PHIM (FRA) ORCID: 0000-0001-8709-9418 - auteur correspondant
  • Pooggin Mikhail, Université de Montpellier (FRA) - auteur correspondant

Source : Cirad-Agritrop (https://agritrop.cirad.fr/610620/)

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