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Thebaud, G.

Publications and source records attributed to Thebaud, G..

6 recordsLinked to original sources

Aphid stylin cuticular proteins contribute to turnip mosaic virus (Potyvirus) transmission

Hundreds of plant viruses are transmitted by aphid vectors, among which non-circulative ones are acquired and inoculated from one host to another within seconds. These viruses are retained on receptors located at the surface of the cuticle of aphid mouthparts. Members of the Potyviridae family are the most abundant RNA viruses infecting plants, and they cause significant economic losses. Among them, viruses of the Potyvirus genus are transmitted by aphids in a stylet-borne manner. Their receptors in aphid stylets remain poorly characterized. Using turnip mosaic virus (TuMV, Potyvirus rapae) as a model, we developed complementary approaches to investigate potyvirus-aphid interactions in three vector species. Immunofluorescence detection and transmission electron microscopy revealed the presence of TuMV in the distal part of aphid maxillary stylets, both in the food canal and on the acrostyle. This cuticular organ houses Stylin proteins, including Stylin-01, the receptor for the cauliflower mosaic virus (Caulimovirus tesselobrassicae). Using CRISPR-Cas9-edited Stylin-01 mutant lines in the pea aphid, we demonstrated that this protein plays an important role in TuMV transmission. Complementary RNA interference silencing experiments revealed that Stylin-04/04bis also mediate TuMV transmission. Furthermore, our findings reveal that targeting simultaneously Stylin-01 and Stylin-04/04bis more strongly impaired the aphids ability to transmit TuMV, suggesting that virus transmission relies on a multi-component stylin interface rather than a single receptor. In conclusion, these results highlight that in complex interactions between potyviruses and their aphid vectors, Stylin proteins are key actors, underscoring their importance in the transmission of stylet-borne viruses. Author summaryPotyviruses are the largest group of plant-infecting RNA viruses and major threats to crops worldwide. Aphids can transmit them within seconds retaining virus particles on their needle-like mouthparts through specific interactions at the stylet surface. However, the identity of the aphid proteins involved in this process has remained unknown. Using turnip mosaic virus (TuMV), a potyvirus with an exceptionnally broad host ranges, we provide evidence of virus retention at the acrostyle, a specialized cuticular microstructure at the tip of aphid stylets. CRISPR-Cas9 stable aphid mutant lines and RNAi-mediated gene silencing revealed that the acrostyle cuticular proteins Stylin-01 and Stylin04/04bis promote TuMV transmission. These findings uncover previously unknown molecular components of the aphid-potyvirus interface and identify potential targets to disrupt virus-vector interaction and virus transmission.

microbiology↗

Symptom observation underestimates co-infections: insight from viral and bacterial diseases in rice fields in Burkina Faso

Co-occurrence of multiple diseases and co-infection of individual plants by various pathogens have potential epidemiological and evolutionary implications. Based on previous information on the co-occurrence of the rice yellow mottle disease (caused by the rice yellow mottle virus, RYMV) and bacterial leaf streak (BLS, due to Xanthomonas oryzae pv. oryzicola, Xoc) in Burkina Faso, and experimental evidence of interactions between the pathogens causing these two diseases, we aimed to monitor the two pathogens more intensively in farmers rice fields. To this purpose, we selected fields showing both types of symptoms to maximize the chance of observing co-infections at the plant scale. We performed observations and sampling in two sites over two consecutive years. Over a global dataset of 1666 samples, 1341 were symptomatic. Although the sampling design aimed to observe co-infections, only 37 of these samples (2.8%) were annotated as presenting both yellow mottle and BLS symptoms. The samples were then subjected to a newly designed molecular detection test that specifically amplifies both the virus (RYMV) and the bacteria (Xo). This revealed that 166 samples, i.e. 12.4% of symptomatic samples, were co-infected by RYMV and Xo, hence showing that symptom observation in the field greatly underestimates co-infection levels. Combining these data with a previously published dataset, we estimated that up to 1-4% of all plants in disease hotspots are simultaneously infected by the two pathogens. Further research on multiple infections would benefit from longitudinal surveys over the crop growing season rather than such a cross-sectional study.

plant biology↗

Dynamics of the rice yellow mottle disease in western Burkina Faso: epidemic monitoring, spatio-temporal variation of viral diversity and pathogenicity in a disease hotspot

The rice yellow mottle virus (RYMV) is a model in plant virus molecular epidemiology and phylogeography, with the reconstruction of historical introduction routes at the scale of the African continent. However, information on patterns of viral prevalence and viral diversity over multiple years at local scale remain scarce, in spite of potential implications for crop protection. Here we describe a five-years monitoring of RYMV prevalence in six sites from western Burkina Faso. This study confirmed one irrigated site as a disease hotspot, and found two rainfed lowland sites with occasional high prevalence levels. Within studied field, a pattern of disease aggregation was evidenced at a five-meter distance, as expected for a mechanically transmitted virus. Next, we monitored RYMV genetic diversity in the irrigated disease hotspot site, revealing a high viral diversity, with the current coexistence of various distinct genetic groups at the site-scale (irrigated perimeter of ca. 520 ha), and also within various specific fields (25 meters side). One genetic lineage, named S1bzn, is the most recently introduced group and increased in frequency over the studied period. Its genome results from a recombination between two other lineages. Finally, experimental work evidenced no differences between three rice varieties cultivated in Burkina Faso in terms of resistance level, and no statistical effect of RYMV genetic group on symptom expression and viral load. We found however, that infection outcome depended on the specific RYMV isolate, with various isolates from the lineage S1bzn found to be particularly aggressive, including one accumulating at highest level. Overall, this study documents a case of high viral prevalence and high viral diversity, with the co-occurrence of divergent genetic lineages at small geographic scale. A recently introduced lineage, that includes viral isolates with high symptoms and accumulation in controlled conditions, could be recently rising though natural selection. Following up the monitoring of RYMV genetic and pathogenic diversity in the area is required to confirm this trend and further understand the factors driving the maintenance of viral diversity at local scale.

evolutionary biology↗

Multi-scale spatial genetic structure of a vector-borne plant pathogen in orchards and wild habitat

Inferring the dispersal processes of vector-borne plant pathogens is a great challenge because the plausible epidemiological scenarios often involve complex spread patterns at multiple scales. European stone fruit yellows (ESFY), a disease caused by Candidatus Phytoplasma prunorum and disseminated via planting material and vectors belonging to the species Cacopsylla pruni, is a major threat for stone fruit production throughout Europe. The spatial genetic structure of the pathogen was investigated at multiple scales by the application of a combination of statistical approaches to a large dataset obtained through the intensive sampling of the three ecological compartments hosting the pathogen (psyllids, wild and cultivated Prunus) in three Prunus-growing regions in France. This work revealed new haplotypes of Ca. P. prunorum, and showed that the prevalence of the different haplotypes of this pathogen is highly uneven between all regions, and within two of them. In addition, we identified a significant clustering of similar haplotypes within a radius of at most 50 km, but not between nearby wild and cultivated Prunus. We also provide evidence that the two species of the C. pruni complex are unevenly distributed but can spread the pathogen, and that infected plants are transferred between production areas. Altogether, this work supports a main epidemiological scenario where Ca. P. prunorum is endemic in, and mostly acquired from, wild Prunus by immature C. pruni (of both species) who then migrate to \"shelter plants\" that epidemiologically connect sites less than 50 km apart by later providing infectious mature C. pruni to their \"migration basins\", which differ in their haplotypic composition. We argue that such multiscale studies would be very useful for other pathosystems.

ecology↗

Heuristic optimisation of the management strategy of a plant epidemic using sequential sensitivity analyses

O_LIOptimisation of management strategies of epidemics is often limited by constraints on experiments at large spatiotemporal scales. A promising approach consists in modelling the biological epidemic process and human interventions, which both impact disease spread. However, few methods enable the simultaneous optimisation of the numerous parameters of sophisticated control strategies. To do so, we propose a heuristic approach based on sequential use of sensitivity analysis. This work is motivated by sharka (caused by Plum pox virus), a vector-borne disease of prunus trees (especially apricot, peach and plum), and its management in orchards, mainly based on surveillance and tree removal.\nC_LIO_LIOur approach is based on three sensitivity analyses which respectively aim to: i) identify the key parameters of a spatiotemporal model simulating disease spread and control; ii) approach optimal values for the key parameters; iii) refine the optimisation.\nC_LIO_LIWe highlight the importance of carefully designing the removal procedure, and propose improved strategies with regard to an economic criterion accounting for both the cost of the different control measures and the benefit generated by productive trees.\nC_LIO_LIWe expect that our general approach will help policymakers to design sustainable and cost-effective strategies for the management of infectious diseases.\nC_LI

epidemiology↗

Estimation of the dispersal distances of an aphid-borne virus in a patchy landscape

Characterising the spatio-temporal dynamics of pathogens in natura is key to ensuring their efficient prevention and control. However, it is notoriously difficult to estimate dispersal parameters at scales that are relevant to real epidemics. Epidemiological surveys can provide informative data, but parameter estimation can be hampered when the timing of the epidemiological events is uncertain, and in the presence of interactions between disease spread, surveillance, and control. Further complications arise from imperfect detection of disease, and from the computationally intractable number of data on individual hosts arising from landscape-level surveys. Here, we present a Bayesian framework that overcomes these barriers by integrating over associated uncertainties in a model explicitly combining the processes of disease dispersal, surveillance and control. Using a novel computationally efficient approach to account for patch geometry, we demonstrate that disease dispersal distances can be estimated accurately in a fragmented landscape when disease control is ongoing. Applying this model to data for an aphid-borne virus (Plum pox virus) surveyed for 15 years over 600 orchards, we obtain the first estimate of the distribution of the flight distances of infectious aphids at the landscape scale. Most infectious aphids leaving a tree land beyond the bounds of a 1-ha orchard (50% of flights terminate within about 90 m). Moreover, long-distance flights are not rare (10% of flights exceed 1 km). By their impact on our quantitative understanding of winged aphids dispersal, these results can inform the design of management strategies for plant viruses, which are mainly aphid-borne.\n\nAuthor SummaryIn spatial epidemiology, dispersal kernels quantify how the probability of pathogen dissemination varies with distance. Spatial models of pathogen spread are sensitive to kernel parameters; yet these parameters have rarely been estimated using field data gathered at relevant scales. Robust estimation is rendered difficult by practical constraints limiting the number of surveyed individuals, and uncertainties concerning their disease status. Here, we present a framework that overcomes these barriers and permits inference for a between-patch transmission model. Extensive simulations show that dispersal kernels can be estimated from epidemiological surveillance data. When applied to such data collected from more than 600 orchards during 15 years of a plant virus epidemic our approach enables the estimation of the dispersal kernel of infectious winged aphids. This kernel is long-tailed, as 50% of the infectious aphids leaving a tree terminate their infectious flight within 90 m and 10% beyond 1 km. This first estimate of flight distances at the landscape scale for aphids-a group of vectors transmitting numerous viruses-is crucial for the science-based design of control strategies targeting plant virus epidemics.

epidemiology↗