Structure-guided mutagenesis of the capsid protein indicates that a nanovirus requires assembled viral particles for systemic infection

PLoS Pathog. 2023 Jan 9;19(1):e1011086. doi: 10.1371/journal.ppat.1011086. eCollection 2023 Jan.

Abstract

Nanoviruses are plant multipartite viruses with a genome composed of six to eight circular single-stranded DNA segments. The distinct genome segments are encapsidated individually in icosahedral particles that measure ≈18 nm in diameter. Recent studies on the model species Faba bean necrotic stunt virus (FBNSV) revealed that complete sets of genomic segments rarely occur in infected plant cells and that the function encoded by a given viral segment can complement the others across neighbouring cells, presumably by translocation of the gene products through unknown molecular processes. This allows the viral genome to replicate, assemble into viral particles and infect anew, even with the distinct genome segments scattered in different cells. Here, we question the form under which the FBNSV genetic material propagates long distance within the vasculature of host plants and, in particular, whether viral particle assembly is required. Using structure-guided mutagenesis based on a 3.2 Å resolution cryogenic-electron-microscopy reconstruction of the FBNSV particles, we demonstrate that specific site-directed mutations preventing capsid formation systematically suppress FBNSV long-distance movement, and thus systemic infection of host plants, despite positive detection of the mutated coat protein when the corresponding segment is agroinfiltrated into plant leaves. These results strongly suggest that the viral genome does not propagate within the plant vascular system under the form of uncoated DNA molecules or DNA:coat-protein complexes, but rather moves long distance as assembled viral particles.

MeSH terms

  • Capsid Proteins / genetics
  • DNA, Viral / genetics
  • Genome, Viral
  • Mutagenesis
  • Nanovirus* / genetics
  • Vicia faba* / genetics
  • Virion / genetics

Substances

  • Capsid Proteins
  • DNA, Viral

Grants and funding

The CBS is a member of the French Infrastructure for Integrated Structural Biology (FRISBI), a national infrastructure supported by the French National Research Agency, ANR (grant ANR‐10‐INBS‐05). This work was supported by Montpellier Université d’Excellence, MUSE, project BLANC-MUSE2020-Multivir, which included a post-doctoral fellowship for E.A.B. This work was supported by the French Agence Nationale de la Recherche (ANR) grant “Nanovirus” (ANR-18-CE92-0028-01). This work used the platforms of the Grenoble Instruct-ERIC centre (ISBG; UAR 3518 CNRS-CEA-UGA-EMBL) within the Grenoble Partnership for Structural Biology (PSB), supported by FRISBI (ANR-10- INBS-05-02) and GRAL, financed within the University Grenoble Alpes graduate school (Ecoles Universitaires de Recherche) CBH-EUR-GS (ANR-17-EURE-0003). The electron microscope facility is supported by the Auvergne-Rhône-Alpes Region, the Fondation Recherche Médicale (FRM), the fonds FEDER and the GIS-Infrastructures en Biologie Sante et Agronomie (IBISA). SB, MY, EP, and MSV acknowledge support from INRAE dpt. SPE, and JLZ from IRD dpt. ECOBIO. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.