Biology subjects

Fargette, D.

Publications and source records attributed to Fargette, D..

5 recordsLinked to original sources

bioRxiv2024

Understanding evolutionary and functional relationships of RNA polymerases in plant and fungal viruses through structural modeling and divergence date estimations

RNA-dependent RNA polymerases (RdRps) are crucial for RNA virus replication and serve as key marker genes for defining deep taxonomic ranks and for understanding viral evolutionary history. Despite their conserved functions and motifs, the high genetic diversity of RdRps complicates precise sequence comparisons across viral families, hindering accurate taxonomic classification of new species. Three-dimensional (3D) RdRp structures can help overcome these challenges through structure-guided alignments. However, such data are rare for myco- and phytoviruses, limiting investigation of their ecological and evolutionary links. In this study, we focused on the highly divergent order Sobelivirales, which includes sobemoviruses infecting plants -- a taxon known for its ancient origin -- and barnaviruses infecting fungi, which remain relatively unknown. Using deep-learning structural modeling, we generated reliable 3D models for 44 sobemoviral and sobelivirad species. Structure-guided alignments, together with new barnaviral and relevant outgroup sequences, enabled robust phylogenetic reconstruction, allowing us to propose revisions of existing viral families and suggest new evolutionary scenarios. Divergence dates were estimated for the first time at this taxonomical rank using the Prisoner of War model, which revealed a divergence of plant and fungal sobelivirads 27.0 {+/-} 10 million years ago -- much more recent than the separation of their respective hosts. This result suggests that cross-kingdom host shifts have contributed more likely to the evolutionary history of Sobelivirales than strict virus-host codivergence. Based on an extended dataset of 127 species, structure and sequence conservation analyses identified molecular signatures of sobeliviral families. These conserved and extented RdRp motifs will facilitate future taxonomic assignments and the development of diagnostic tools. Our interdisciplinary approach, integrating structure modeling and divergence dating, offers new insights into the evolutionary divergence of plant and fungal viruses, with potential applications to other viral orders and families. Author summaryRNA-dependent RNA polymerases (RdRps) are essential for RNA virus replication and serve as important markers for classifying viruses and understanding their evolution. However, with metagenomic studies that rapidly expand the known diversity of RNA viruses, it is increasingly difficult to compare highly divergent RdRps and accurately classify new species. When available, 3D structures of RdRps can help overcome this challenge through structure-guided alignments. Here, we focused on the highly divergent order Sobelivirales, which groups phytoviruses and mycoviruses. Deep-learning models were used to generate reliable 3D structures for 44 representative viral species. Structure-guided alignments combined with the identification of new barnaviruses and outgroups allowed us to build a more accurate viral phylogeny. Based on this finding, we proposed updates to existing viral families and genera within the order Sobelivirales. We estimated divergence dates using a model that previously uncovered the ancient origins of sobemovirus. Notably, we provided the first estimate of when these plant and fungal viruses diverged [~]27.0 {+/-} 10 million years ago, suggesting cross-kingdom host shifts rather than strict virus-host codivergence. We also identified molecular signatures that are useful for future virus classification and diagnosis, with potential applications to other viral groups.

evolutionary biology↗

bioRxiv2024

Grains, trade and war in the multimodal transmission of Rice yellow mottle virus: an historical and phylogeographical retrospective

Rice yellow mottle virus (RYMV) is a major pathogen of rice in Africa. RYMV has a narrow host range limited to rice and a few related poaceae species. We explore the links between the spread of RYMV in East Africa and rice history since the second half of the 19th century. The phylogeography of RYMV in East Africa was reconstructed from coat protein gene sequences (ORF4) of 335 isolates sampled over two million square kilometers between 1966 and 2020. Dispersal patterns obtained from ORF2a and ORF2b, and full-length sequences converged to the same scenario. The following imprints of rice cultivation on RYMV epidemiology were unveiled. RYMV emerged in the middle of the 19th century in the Eastern Arc Mountains where slash-and-burn rice cultivation was practiced. Several spillovers from wild hosts to cultivated rice occurred. RYMV was then rapidly introduced into the adjacent large rice growing Kilombero valley. Harvested seeds are contaminated by debris of virus infected plants that subsist after threshing and winnowing. Long-distance dispersal of RYMV is consistent (i) with rice introduction along the caravan routes from the Indian Ocean Coast to Lake Victoria in the second half of the 19th century, (ii) seed movement from East Africa to West Africa at the end of the 19th century, from Lake Victoria to the north of Ethiopia in the second half of the 20th century and to Madagascar at the end of the 20th century, (iii) and, unexpectedly, with rice transport at the end of the First World War as a troop staple food from the Kilombero valley towards the South of Lake Malawi. Overall, RYMV dispersal was associated to a broad range of human activities, some unsuspected. Consequently, RYMV has a wide dispersal capacity, its dispersal metrics estimated from phylogeographic reconstructions are similar to those of highly mobile zoonotic viruses. Author summaryRice yellow mottle virus (RYMV) poses a major threat to rice production in Africa. We explored through a multidisciplinary approach the links between the history of rice in East Africa since the second half of the 19th century and the spread of RYMV. The results illuminate the causes of RYMV diffusion. We show the role of long-distance caravan trade, the impact of the First World War and the consequences of seed exchange in the dispersal of RYMV. The paradoxical role of seeds in the spread of RYMV - which is vector transmitted and not seed transmitted - is explained in the light of rice biology and agronomy. Overall, this study reveals the wide range of transmission ways, some unexpected, in the dispersal of plant viruses. It also highlights the role of human transmission of pathogens, even vector-borne, and sheds light on the risk of transmission of RYMV and of other plant viruses from Africa to other continents.

evolutionary biology↗

bioRxiv2024

Modeling the velocity of evolving lineages and predicting dispersal patterns

Accurate estimation of the dispersal velocity or speed of evolving organisms is no mean feat. In fact, existing probabilistic models in phylogeography or spatial population genetics generally do not provide an adequate framework to define velocity in a relevant manner. For instance, the very concept of instantaneous speed simply does not exist under one of the most popular approaches that models the evolution of spatial coordinates as Brownian trajectories running along a phylogeny (Lemey et al., 2010). Here, we introduce a new family of models - the so-called "Phylogenetic Integrated Velocity" (PIV) models - that use Gaussian processes to explicitly model the velocity of evolving lineages instead of focusing on the fluctuation of spatial coordinates over time. We describe the properties of these models and show an increased accuracy of velocity estimates compared to previous approaches. Analyses of West Nile virus data in the U.S.A. indicate that PIV models provide sensible predictions of the dispersal of evolving pathogens at a one-year time horizon. These results demonstrate the feasibility and relevance of predictive phylogeography in monitoring epidemics in time and space.

evolutionary biology↗

bioRxiv2024

How fast are viruses spreading in the wild?

Genomic data collected from viral outbreaks can be exploited to reconstruct the dispersal history of viral lineages in a two-dimensional space using continuous phylogeographic inference. These spatially explicit reconstructions can subsequently be used to estimate dispersal metrics allowing to unveil the dispersal dynamics and evaluate the capacity to spread among hosts. Heterogeneous sampling intensity of genomic sequences can however impact the accuracy of dispersal insights gained through phylogeographic inference. In our study, we implement a simulation framework to evaluate the robustness of three dispersal metrics -- a lineage dispersal velocity, a diffusion coefficient, and an isolation-by-distance signal metric -- to the sampling effort. Our results reveal that both the diffusion coefficient and isolation-by-distance signal metrics appear to be robust to the number of samples considered for the phylogeographic reconstruction. We then use these two dispersal metrics to compare the dispersal pattern and capacity of various viruses spreading in animal populations. Our comparative analysis reveals a broad range of isolation-by-distance patterns and diffusion coefficients mostly reflecting the dispersal capacity of the main infected host species but also, in some cases, the likely signature of rapid and/or long-distance dispersal events driven by human-mediated movements through animal trade. Overall, our study provides key recommendations for the lineage dispersal metrics to consider in future studies and illustrates their application to compare the spread of viruses in various settings.

evolutionary biology↗

bioRxiv2023

Revisiting the origins of the Sobemovirus genus: a case for ancient origins of plant viruses

The discrepancy between short- and long-term rate estimates, known as the time-dependent rate phenomenon (TDRP), poses a challenge to extrapolating evolutionary rates over time and reconstructing evolutionary history of viruses. The TDRP reveals a decline in evolutionary rate estimates with the measurement timescale, explained empirically by a power-law rate decay, notably observed in animal and human viruses. A mechanistic evolutionary model, the Prisoner of War (PoW) model, has been proposed to address TDRP in viruses. Although TDRP has been studied in animal viruses, its impact on plant virus evolutionary history remains largely unexplored. Here, we investigated the consequences of TDRP in plant viruses by applying the PoW model to reconstruct the evolutionary history of sobemoviruses, plant pathogens with significant importance due to their impact on agriculture and plant health. Our analysis showed that the Sobemovirus genus dates back over four million years, indicating an ancient origin. We found evidence that supports deep host jumps to Poaceae, Fabaceae, and Solanaceae occurring between tens to hundreds of thousand years ago, followed by specialization. Remarkably, the TDRP-corrected evolutionary history of sobemoviruses was extended far beyond previous estimates that had suggested their emergence during the Neolithic period. By incorporating sequences collected through metagenomic analyses, the resulting phylogenetic tree showcases increased genetic diversity, reflecting a deep history of sobemovirus species with major radiation events taking place during the Neolithic period, suggesting rapid diversification in that period. Our findings make a case for the possibility of deep evolutionary origins of plant viruses.

evolutionary biology↗