Identification and Molecular Characterization of a Novel Hordeivirus Associated With Yellow Mosaic Disease of Privet (Ligustrum vulgare) in Europe.

Reynard, Jean-Sébastien; Turco, Silvia; Brodard, Justine; Kellenberger, Isabelle; Maclot, François; Schumpp, Olivier; Gugerli, Paul; Pooggin, Mikhail M

doi:10.3389/fmicb.2021.723350

Article (Scientific journals)

Identification and Molecular Characterization of a Novel Hordeivirus Associated With Yellow Mosaic Disease of Privet (Ligustrum vulgare) in Europe.

Reynard, Jean-Sébastien; Turco, Silvia; Brodard, Justine et al.

2021 • In Frontiers in Microbiology, 12, p. 723350

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/291770

DOI
10.3389/fmicb.2021.723350

PubMed
34646247

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Keywords :

Hordeivirus; Ligustrum; distribution; genome; phylogeny; siRNAs; transmission; virions; Microbiology; Microbiology (medical)

Abstract :

[en] Wild plants serve as a large reservoir of known and yet-unknown viruses and as a source of viral pathogens of cultivated plants. Yellow mosaic disease of forest shrub Ligustrum vulgare (privet) was recurrently observed in Europe for more than 100 years. Using a universal virus identification approach based on deep sequencing and de novo assembly of viral small interfering (si)RNAs we identified a causative agent of this disease in Switzerland and reconstructed its complete 3-segmented RNA genome. Notably, a short 3'-terminal common region (CR) attached to each segment via a ∼53-71 nucleotide poly(A) tract, as determined by RT-PCR sequencing, was initially identified as an orphan siRNA contig with conserved tRNA-like secondary structure. Phylogenomic analysis classified this virus as a novel member in the genus Hordeivirus of family Virgaviridae, which we named ligustrum mosaic virus (LigMV). Similar to other hordeiviruses, LigMV formed rod-shape virions (visualized by electron microscopy), was transmitted through seeds and could also be mechanically transmitted to herbaceous hosts Chenopodium quinoa and Nicotiana benthamiana. Blot hybridization analysis identified genomic and subgenomic RNAs, sharing the 3'-CR and likely serving as monocistronic mRNAs for seven evolutionarily-conserved viral proteins including two subunits of viral RNA-dependent RNA polymerase, coat protein, triple gene block proteins mediating viral movement and cysteine-rich suppressor of RNA silencing. Analysis of size, polarity, and hotspot profiles of viral siRNAs suggested that they are produced by the plant antiviral Dicer-like (DCL) proteins DCL2 and DCL4 processing double-stranded intermediates of genomic RNA replication. Whole genome sequencing of French and Austrian isolates of LigMV revealed its genetic stability over a wide geographic range (>99% nucleotide identity to Swiss isolates and each other), suggesting its persistence and spread in Europe via seed dispersal.

Disciplines :

Environmental sciences & ecology
Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Reynard, Jean-Sébastien; Virology-Phytoplasmology Laboratory, Agroscope, Nyon, Switzerland

Turco, Silvia; Department of Environmental Sciences, Botany, University of Basel, Basel, Switzerland

Brodard, Justine; Virology-Phytoplasmology Laboratory, Agroscope, Nyon, Switzerland

Kellenberger, Isabelle; Virology-Phytoplasmology Laboratory, Agroscope, Nyon, Switzerland

Maclot, François ; Université de Liège - ULiège

Schumpp, Olivier; Virology-Phytoplasmology Laboratory, Agroscope, Nyon, Switzerland

Gugerli, Paul; Virology-Phytoplasmology Laboratory, Agroscope, Nyon, Switzerland

Pooggin, Mikhail M; PHIM Plant Health Institute, University of Montpellier, INRAE, CIRAD, IRD, Institute Agro, Montpellier, France

Language :

English

Title :

Identification and Molecular Characterization of a Novel Hordeivirus Associated With Yellow Mosaic Disease of Privet (Ligustrum vulgare) in Europe.

Publication date :

2021

Journal title :

Frontiers in Microbiology

eISSN :

1664-302X

Publisher :

Frontiers Media S.A., Switzerland

Volume :

Pages :

723350

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.frontiersin.org/articles/10.3389/fmicb.2021.723350/full

Name of the research project :

Seventh Framework Programme

Funders :

SNF - Schweizerischer Nationalfonds zur Förderung der wissenschaftlichen Forschung [CH]
INRA - Institut National de la Recherche Agronomique [FR]

Funding text :

This work was funded by the FP7 People Marie-Curie Actions grant 608422 and INRAE SPE department ViroMix grant to MP, and by Swiss National Science Foundation grant IZCNZ0-174857 to OS and Laurent Farinelli.We thank Nathalie Dubuis, Larisa Grosu Duchene, and Victor Golyaev for technical assistance.

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