Molecular and cellular aspects of the life cycle of multipartite viruses: nanoviruses

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Emerging plant viruses are a threat worldwide. Studying their life cycles in details is a prerequisite to reveal alternative control strategies. We will target the family Nanoviridae for both practical and fundamental reasons: i) it represents a huge threat for Musaceae crop (genus Babuvirus) and for legumes (genus Nanovirus), and ii) it has adopted the enigmatic “multipartite” organization, with its genome composed of several nucleic acid segments each encapsidated individually. Nanoviruses being multipartite viruses with the highest number of genome segments described thus far, they are perfect models to investigate processes that might be specific to this viral genomic architecture most frequently adopted by plant viruses. In particular, how such viruses can efficiently infect a high proportion of cells/hosts with at least one copy of each of their numerous genome segments remains elusive. It is deemed impossible in the literature that actually questions the conceptual frame with which we try to comprehend the multipartite viral systems. Consistently, we recently showed that a nanovirus do not function in a way that fits the current concepts in virology. The virus spreads distinct genome segments in distinct individual cells of the host. These segments functionally complement across cells and thereby define a pluricellular way of life. This unprecedented discovery in virology now requires in depth investigation to decipher the mechanisms allowing such a surprising viral lifestyle. More specifically the Krenz group analyzes the viral proteins role during virus-host interactions, while the Blanc group studies the within-host viral population dynamics and the virus-vector interactions during plant-to-plant transmission. Through this project, we will join forces to study the full lifecycle. We propose to decipher the biochemical and biological properties of various nanoviral gene products interacting with host plants and aphid vectors. We aim to understand how distinct viral genome segments initially expressed in distinct plant cells actually function, how they can communicate and complement at a distance and at a supra-cellular scale. We will analyze the properties of the viral gene products with a focus on those with yet unknown function, and on properties that could be involved in trafficking among cells for complementation. Likewise, we will strive to understand how virus particles successfully travel through the body of their aphid vectors, ensuring that all segments are acquired, transported across aphid’s cell barriers, and inoculated together. Thus, beyond the urgent need to better understand the biology of nanoviruses, an emerging threat worldwide, another ambitious goal of this project is to decipher the means by which a multipartite virus can sustain a pluricellular lifestyle, and thereby definitely coin this discovery as a new research horizon in plant virology and beyond.