Debonneville, C. | Search bioRxiv

bioRxiv2026

Integrated field and laboratory assessment of Swiss grapevine cultivar susceptibility to flavescence doree reveals a central role for plant-vector interactions

Cultivar susceptibility strongly influences the epidemiology of vector-borne plant diseases, and understanding cultivar-specific variation can inform management strategies. This is particularly relevant for flavescence doree, an incurable grapevine disease associated with a phytoplasma and transmitted by the leafhopper Scaphoideus titanus. In this study, we investigated the susceptibility of the main Swiss varieties, by combining controlled insect-mediated inoculation experiments with complementary field analyses conducted at progressively finer spatial scales. Together, these approaches allowed us to compare both infection probability and phytoplasma relative titre under standardised transmission conditions with disease incidence and relative titre under natural epidemiological conditions. For most cultivars, laboratory results were broadly consistent with field observations. However, a marked discrepancy emerged in the relative infection pattern between the two main grapevine cultivars grown in Switzerland: Chasselas and Pinot Noir. Under controlled conditions, they did not differ significantly in either their probability of infection or the phytoplasma relative titre, indicating no detectable difference in susceptibility to phytoplasma infection. In contrast, Pinot Noir consistently showed higher disease incidence than Chasselas under natural conditions. This pattern was observed across all spatial scales examined, from regional surveys to neighbouring vineyard plots, and was mirrored by higher phytoplasma relative titres. Importantly, under controlled conditions, S. titanus mortality during the one-week inoculation period was significantly higher on Chasselas than on Pinot Noir, indicating that Chasselas may provide a less favourable host for S. titanus. Together, these findings support the hypothesis that differences in field disease incidence between these cultivars may arise from differences in vector performance rather than intrinsic susceptibility to phytoplasma infection. This highlights the importance of considering plant-vector interactions, alongside susceptibility to infection, when assessing cultivar-specific vulnerability to vector-borne plant diseases.

plant biology↗

bioRxiv2024

From insect endosymbiont to phloem colonizer: comparative genomics unveils the lifestyle transition of phytopathogenic Arsenophonus strains

Bacteria infecting the plant phloem represent a growing threat worldwide. While these organisms often resist in vitro culture, they multiply both in plant sieve elements and hemipteran vectors. Such cross-kingdom parasitic lifestyle has emerged in diverse taxa via distinct ecological routes. In the genus Arsenophonus, the phloem pathogens Candidatus Arsenophonus phytopathogenicus (Ap) and Ca. Phlomobacter fragariae (Pf) have evolved from insect endosymbionts, but the genetic mechanisms underlying this transition have not been explored. To fill this gap, we obtained the genomes of both strains from insect host metagenomes. The resulting assemblies are highly similar in size and functional repertoire, rich in viral sequences, and closely resemble the genomes of several facultative endosymbiotic Arsenophonus strains of sap-sucking hemipterans. However, a phylogenomic analysis demonstrated distinct origins, as Ap belongs to the "Triatominarum" clade whereas Pf represents a distant species. We identified a set of orthologs encoded only by Ap and Pf in the genus, including hydrolytic enzymes likely targeting plant substrates. In particular, both bacteria encode plant cell-wall degrading enzymes and cysteine peptidases related to xylellain, a papain-like peptidase from Xylella fastidiosa, for which close homologs are found in diverse proteobacteria infecting the plant vasculature. In silico predictions and expression analyses further support a role during phloem colonization for several of the shared orthologs. We conclude that the double emergence of phytopathogenicity in Arsenophonus may have been mediated by a few horizontal gene transfer events, involving genes first acquired from other proteobacteria including phytopathogens. ImportanceWe investigate the genetic mechanisms of a transition in bacterial lifestyle. We focus on two phloem pathogens belonging to the genus Arsenophonus: Ca. Arsenophonus phytopathogenicus and Ca. Phlomobacter fragariae. Both bacteria cause economically significant pathologies, and they have likely emerged among facultative insect endosymbionts. Our genomic analyses show that both strains are highly similar to other strains of the genus associated with sap-sucking hemipterans, indicative of a recent lifestyle shift. Importantly, although the phytopathogenic Arsenophonus strains belong to distant clades, they share a small set of orthologs unique in the genus pangenome. We provide evidence that several of these genes produce hydrolytic enzymes that are secreted and target plant substrates. The acquisition and exchange of these genes may thus have played a pivotal role in the lifestyle transition of the phytopathogenic Arsenophonus strains..

microbiology↗