The bacterium Xylella fastidiosa re-emerged as a plant pathogen of global importance in 2013 when it was first associated with an olive tree disease epidemic in Italy. The current threat to Europe and the Mediterranean basin, as well as other world regions, has increased as multiple X. fastidiosa genotypes have now been detected in Italy, France, and Spain. Although X. fastidiosa has been studied in the Americas for more than a century, there are no therapeutic solutions to suppress disease development in infected plants. Furthermore, because X. fastidiosa is an obligatory plant and insect vector colonizer, the epidemiology and dynamics of each pathosystem are distinct. They depend on the ecological interplay of plant, pathogen, and vector and on how interactions are affected by biotic and abiotic factors, including anthropogenic activities and policy decisions. Our goal with this review is to stimulate discussion and novel research by contextualizing available knowledge on X. fastidiosa and how it may be applicable to emerging diseases.

To study the role of wild areas around the vineyards in the epidemiology of flavescence dorée (FD) and track the origin of new foci, two phytoplasma genetic markers, dnaK and malG, were developed for FD phytoplasma (FDp) characterization. The two genes and the vmpA locus were used to genetically characterize FDp populations at seven agroecosystems of a wine-growing Italian region. Vitis vinifera, “gone-wild” V. vinifera and rootstocks, Clematis spp., and Scaphoideus titanus adults were sampled within and outside the vineyards. A range of genotypes infecting the different hosts of the FDp epidemiological cycle was found. Type FD-C isolates were fairly homogeneous compared to type FD-D ones. Most of the FD-D variability was correlated with the malG sequence, and a duplication of this locus was demonstrated for this strain. Coinfection with FD-C and FD-D strains was rare, suggesting possible competition between the two. Similar levels of FDp genetic variation recorded for grapevines or leafhoppers of cultivated and wild areas and co-occurrence of many FDp genotypes inside and outside the vineyards supported the idea of the importance of wild or abandoned Vitis plants and associated S. titanus insects in the epidemiology of the disease. Genetic profiles of FDp found in Clematis were never found in the other hosts, indicating that this species does not take part in the disease cycle in the area. Due to the robustness of analyses using dnaK for discriminating between FD-C and FD-D strains and the high variability of malG sequences, these are efficient markers to study FDp populations and epidemiology at a small geographical scale. IMPORTANCE Flavescence dorée, a threatening disease of grapevine caused by FD phytoplasma (FDp), is distributed within the most important wine-producing areas of Europe and has severe effects on both vineyard productivity and landscape management. FDp is a quarantine pest in Europe, and despite the efforts to contain the pathogen, the disease is still spreading. In this work, new genetic markers for the fine genetic characterization of FDp at local scale are presented. Our findings improve the knowledge of FDp epidemiological cycle and offer the possibility of tracking the route of the FDp infection. In particular, due to its high genetic variability, one of the newly developed markers could be sufficient to track the origin of new infection foci, either from the wild areas or from nurseries.

The meadow spittlebug, Philaenus spumarius (Linnaeus) (Hemiptera: Aphrophoridae), is a vector of the plant pathogen Xylella fastidiosa; however, its role in recent outbreaks of Pierce’s disease of grapevine (PD) in California is unclear. While the phenology and ecology of P. spumarius can help determine its contributions to PD epidemics, both remain poorly described in the North Coast vineyards of California. We assessed the phenology of P. spumarius in the region. Spittlemasses were first observed in February or March, while the emergence of adult spittlebugs did not occur until April or May depending on the year. Analysis of sweep and trap data from 2016 to 2018 revealed significant effects of survey month, vineyard site, and year on adult abundance in sweep and trap surveys. Spittlebug adults were present in the vineyards from April until December, with the greatest number of adults by sweep net in May or June, whereas adults on traps peaked between July and November. Analysis of natural infectivity in groups of field-collected spittlebug adults showed significant difference in transmission rates among months. Spittlebugs successfully transmitted Xylella fastidiosa (Wells) (Xanthomonadales: Xanthomonadaceae) to potted grapevines between July and December. The greatest risk of X. fastidiosa transmission by P. spumarius was in December (60%) followed by October (30%). However, the infectivity patterns of the meadow spittlebug did not align with the historical paradigm of California North Coast PD. We discuss alternative hypotheses in which P. spumarius could play a role in the epidemiology of this disease.

Quantitative estimates of vector populations and their infectivity in the wild and in cultivated compartments of agroecosystems have been carried out to elucidate the role of the wild compartment in the epidemiology of Flavescence dorée (FD). Seven sites were selected for the investigations in the Piedmont Region of Italy. They were characterized by a high variety of agricultural and ecological landscape features, and included a vineyard surrounded by wild vegetation. In order to describe abundance and prevalence of FD-infected vectors in the cultivated and wild compartments of the vineyard agroecosystem, adults of Scaphoideus titanus were collected by yellow sticky traps inside and outside the vineyard over the period July 10th–September 9th, 2015. They were counted and singly analyzed for the presence of FD phytoplasmas by PCR. Multifactorial correlations among vector population level, prevalence of infected insects inside and outside the vineyards, disease prevalence in cultivated and wild Vitis plants, and location of wild Vitis plants with respect to the vineyard were analyzed. Abundance of S. titanus adults significantly decreased from the end of July onwards, particularly inside the vineyard (average range 22.7 ± 2.5 insects/trap). Percentage of FD-positive S. titanus was significantly higher outside the vineyard (up to 48% on average) compared to inside the vineyard (up to 34% on average), and increased during the season in both compartments.

We report the first known incidence of two parasitoid species of the invasive pest, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), in the United States (US). The discovery of Ganaspis brasiliensis (Ihering) (Hymenoptera: Figitidae) and Leptopilina japonica (Novković & Kimura) (Hymenoptera: Figitidae) in northwestern Washington State (US) was made shortly after their discovery in nearby southwestern British Columbia (Canada), indicating that contiguous populations of these species are established in both countries. The first specimen of L. japonica from Washington was collected in the fall of 2020, when it was found in a rice wine/orange juice trap deployed to survey for Vespa mandarinia Smith (Hymenoptera: Vespidae). Subsequent examination of trap contents from the 2020–2021 seasons indicated the presence of both L. japonica and G. brasiliensis. In September of 2021, live collections of both G. brasiliensis and L. japonica were made, reared from D. suzukii-infested Himalayan blackberry in Whatcom County, WA. Adult parasitoid identifications were based on morphology and COI DNA barcodes. All sequenced specimens to date from Washington and British Columbia belong to the G1 group of G. brasiliensis, the only group approved for release as a classical biological control agent in the US. This study provides an example of how even small changes in the geographic range of a natural enemy, now extending across an international border, may have significant consequences for the future of a biological control program.

Spotted-wing drosophila (SWD), Drosophila suzukii Matsumura (Diptera: Drosophilidae), is an invasive pest of thin-skinned fruits in the United States. Monitoring traps are an integral part of SWD integrated pest management, allowing early detection and timely management of this pest. An ideal monitoring trap should be easy to use, effective in capturing SWD, sensitive and selective to male SWD which are easy to identify due to their spotted wings, and able to predict fruit infestation from trap captures. Deli-cup-based liquid traps (grower standard), which make in-situ observations difficult, were compared with red-panel sticky traps, both baited with commercial lures (Scentry, Trécé Broad-Spectrum (BS), and Trécé High-Specificity (HS)), across several US states in blueberries (lowbush and highbush), blackberry, raspberry, and cherry crops during 2018 and 2021. Results showed that red-panel traps effectively captured SWD, were able to detect male SWD early in the season while also being selective to male SWD all season-long, and in some cases linearly related male SWD trap captures with fruit infestation. Scentry and Trécé BS lures captured similar numbers of SWD, though Trécé BS and Trécé HS were more selective for male SWD in red panel traps than liquid traps in some cases. In conclusion, due to its ease of use with less processing time, red-panel traps are promising tools for detecting and identifying male SWD in-situ and for predicting fruit infestation. However, further research is needed to refine the trap captures and fruit infestation relationship and elucidate the trap-lure interactions in berry and cherry crops.

Although Aphrophora nr. permutata (Hemiptera: Aphrophoridae) is a reported vector of the plant pathogen Xylella fastidiosa (Wells) (Xanthomonadales: Xanthomonadaceae), its ecology and role in Pierce’s disease dynamics in coastal California vineyards are poorly understood. From 2016 to 2020, we surveyed the abundance of A. nr. permutata nymphs among potential host plants along the vineyard floor, the vineyard edges, and adjacent vegetation in vineyards in Napa and Sonoma county. In 2019 and 2020, vineyards adjacent to woodland habitat hosted larger A. nr. permutata populations than those next to riparian habitat, while in 2017 and 2018, the nymphal populations were similar among riparian and woodland sites. Among 2020 plant cover taxa, nymph abundance was positively associated with Helminthotheca echioides, Vicia sativa, and Daucus carota cover and negatively associated with Taraxacum officinale cover. In 2018 and 2019, we also tracked early-season occurrence and development of A. nr. permutata nymphs among potential host plants. Analyses showed a significant effect of site, year, and plant taxa on the first detection of nymphs and a significant effect of site and year on the estimated development time between first and fifth instars. In 2019, we conducted grapevine to grapevine X. fastidiosa transmission experiments with individuals and groups of five A. nr. permutata adults. In the transmission experiment, 5% (3 of 60) individual A. nr. permutata and 7.7% (1 of 13) of groups successfully transmitted X. fastidiosa. This study provides preliminary evidence of potential host plant associations with A. nr. permutata abundance and phenology that should be explored further with field and greenhouse-based approaches.

Pierce’s disease is of major concern for grapevine ( Vitis vinifera ) production wherever the bacterial pathogen Xylella fastidiosa and its vectors are present. Long-term management includes the deployment of resistant grapevines such as those containing the PdR1 locus from the wild grapevine species Vitis arizonica , which do not develop Pierce’s disease symptoms upon infection. However, little is understood about how the PdR1 locus functions to prevent disease symptom development. Therefore, we assessed the concentrations of plant defense-associated compounds called phenolics in healthy and X . fastidiosa -infected PdR1 -resistant and susceptible grapevine siblings over time. Soluble foliar phenolic levels, especially flavonoids, in X . fastidiosa -infected PdR1 -resistant grapevines were discovered to be significantly lower than those in infected susceptible grapevines. Therefore, it was hypothesized that PdR1 -resistant grapevines, by possessing lowered flavonoid levels, affects biofilm formation and causes reduced X . fastidiosa intra-plant colonization, thus limiting the ability to increase pathogen populations and cause Pierce’s disease. These results therefore reveal that differences in plant metabolite levels might be a component of the mechanisms that PdR1 utilizes to prevent Pierce’s disease.