Grapevine leafroll-associated virus 3 (GLRaV-3) is associated with the economically damaging grapevine leafroll disease, and is transmitted in a semi-persistent manner by several mealybug species. We performed the first controlled field study of vector-mediated inoculations with GLRaV-3 in a commercial vineyard with previously asymptomatic vines, and monitored the vines during four growing seasons. We then compared the outcome of vector-mediated inoculations in the field study to an analogous laboratory study. In the vineyard, about half of all inoculated plants became infected with GLRaV-3, fewer than in the controlled laboratory inoculations. Mealybugs had lower settling and feeding success in the field than in the laboratory inoculations. Our study suggests that laboratory studies may overestimate transmission efficiency. All successfully inoculated vineyard plants first became symptomatic one growing season after inoculations, and berry quality declined within one year after inoculations. Vineyard plants were effective virus sources one year after inoculations. Our findings generally indicate that newly symptomatic vines in commercial vineyards probably became infected during the previous growing season, and a decline in berry quality can be expected during the same year in which symptoms appear.

Grapevine leafroll disease (GLD) is caused by a complex of vector-borne virus species in the family Closteroviridae. GLD is present in all grape-growing regions of the world, primarily affecting wine grape varieties. The disease has emerged in the last two decades as one of the major factors affecting grape fruit quality, leading to research efforts aimed at reducing its economic impact. Most research has focused on the pathogens themselves, such as improved detection protocols, with limited work directed toward disease ecology and the development of management practices. Here we discuss the ecology and management of GLD, focusing primarily on Grapevine leafroll-associated virus 3, the most important virus species within the complex. We contextualize research done on this system within an ecological framework that forms the backbone of the discussion regarding current and potential GLD management strategies. To reach this goal, we introduce various aspects of GLD biology and ecology, followed by disease management case studies from four different countries and continents (South Africa, New Zealand, California-USA, and France). We review ongoing regional efforts that serve as models for improved strategies to control this economically important and worldwide disease, highlighting scientific gaps that must be filled for the development of knowledge-based sustainable GLD management practices.

Some diseases manifest as one characteristic set of symptoms to the host, but can be caused by multiple pathogens. Control treatments based on plant symptoms can make it difficult to effectively manage such diseases, as the biology of the underlying pathogens can vary. Grapevine leafroll disease affects grapes worldwide, and is associated with several viral species in the family Closteroviridae. Whereas some of the viruses associated with this disease are transmitted by insect vectors, others are only graft-transmissible. In three regions of California, we surveyed vineyards containing diseased vines and screened symptomatic plants for all known viral species associated with grapevine leafroll disease. Relative incidence of each virus species differed among the three regions regions, particularly in relation to species with known vectors compared with those only known to be graft-transmitted. In one region, the pathogen population was dominated by species not known to have an insect vector. In contrast, populations in the other surveyed regions were dominated by virus species that are vector-transmissible. Our survey did not detect viruses associated with grapevine leafroll disease at some sites with characteristic disease symptoms. This could be explained either by undescribed genetic diversity among these viruses that prevented detection with available molecular tools at the time the survey was performed, or a misidentification of visual symptoms that may have had other underlying causes. Based on the differences in relative prevalence of each virus species among regions and among vineyards within regions, we expect that region and site-specific management strategies are needed for effective disease control.