Grapevine flavescence dorée symptoms © Sandrine Eveillard

Grapevine flavescence dorée

Origin of the disease

Genomic studies have demonstrated that the phytoplasma strains responsible for flavescence dorée originated in Europe and already existed in wild plants such as alder and clematis before being introduced into grapevines. The insect vector, Scaphoideus titanus, is from the United States and was likely introduced in France when American rootstocks were imported as a part of the fight against downy mildew and phylloxera in the early twentieth century. Scaphoideus titanus is largely responsible for the rapid spread of flavescence dorée in France and in Europe. 

By Pascale Mollier - Julien Chuche - Denis Thiéry - Daciana Papura - Sylvie Malembic - Alain Blanchard - Xavier Foissac, translated by Daniel McKinnon
Updated on 09/06/2016
Published on 03/26/2013

Clematis infected by flavescence dorée. © INRA, Jean-Luc Danet
Clematis infected by flavescence dorée © INRA, Jean-Luc Danet

Flavescence dorée is a European disease, originally present in wild plants such as alder and clematis. It was only with the recent introduction from North America of the vector, Scaphoideus titanus, that flavescence dorée was able to rapidly spread into the Vitis vinifera grapevine.

Flavescence dorée pre-existed in European wild plants

Genetic markers of the flavescence dorée phytoplasma have been isolated using its genome sequencing. The markers enable the study of the molecular diversity in flavescence dorée phytoplasma to better understand the origin of the disease, to identify new reservoirs and to follow the spread of different strains into grapevines. The studies revealed that flavescence dorée was originally from Europe and that the original host reservoirs were wild plants such as alder and clematis. Strains of the three phytoplasma genetic groups responsible for flavescence dorée (FD 1, 2 and 3) are identical or very similar to certain isolates occurring in alder. A German research team demonstrated that the phytoplasma may have been accidentally transmitted to grapevines by another leafhopper species, Oncopsis alni. Phytoplasma identical to FD3 type strains have also been identified in white clematis growing near vineyard plots, but also in non-winegrowing areas in Italy and the Balkans. Italian studies noted the presence in the undergrowth of insects that visit clematis and the occasional presence of Scaphoideus titanus on clematis plants. A planthopper species, Dictyophara europaea, capable of carrying phytoplasma identical to the FD3 strain and of transmitting it to grapevines has also been observed in such ecosystems.

However grapevines may have been infected initially, the disease was first identified in 1949 in Armagnac. In that year, flavescence dorée was limited to a small number of vines in a confined geographic area.

S. titanus would have then accelerated the transmission of flavescence dorée from vine to vine. However, the low genetic diversity of the strains, the similar levels of virulence among them and the rapid spread to other vineyards suggest that the main strains were first spread by the transport of contaminated plant material and then by natural transmission via the insect vector.

S. titanus, the main vector, arrived in Europe at the start of the twentieth century

In examining historical records, it is probable that the S. titanus leafhopper was introduced accidentally from North America to Europe at the start of the twentieth century. In its original range, S. titanus is rarely observed on cultivated grapevines. The species is mostly captured in the wild, in general on wild Vitis species. In Europe, S. titanus was first observed in 1958 in a vineyard in southwestern France before rapidly spreading over a large portion of France’s total vineyard area and then to Italy, Switzerland and swaths of Southern and Central Europe. Genetic characterisation of American and European S. titanus populations revealed that, with a single main haplotype in Europe, European populations descend from a single introduction from the United States and that the winegrowing region in the American East Coast was the most likely origin of European populations.

The introduction of the leafhopper may be linked to the considerable imports of vine wood from the United States as a part of the fight against downy mildew and phylloxera epidemics happening in Europe, for the most part before 1930. During this time, a large number of S. titanus eggs were likely introduced on a number of occasions and were likely all imported from the same region in the northern United States. Identifying the colonisation route into Europe will be an essential element in assessing the impact of control methods designed to stop the spread of introduced populations.

References

- Arnaud, G., Malembic-Maher, S., Salar, P., Bonnet, P., Maixner, M., Marcone, C., Boudon-Padieu, E. et Foissac, X. 2007. Multilocus sequence typing confirms the close genetic inter-relatedness between three distinct flavescence dorée phytoplasma strain clusters and group 16SrV phytoplasmas infecting grapevine and alder in Europe. Applied and Environmental Microbiology,73: 4001-4010.

- Papura, D., Giresse, X., Delmotte, F., Danet, J. L., van Helden, M., Foissac, X. et Malembic-Maher, S. 2009. Comparing the spatial genetic structures of the Flavescence dorée phytoplasma and its leafhopper vector Scaphoideus titanus. Infection Genetics and Evolution,9: 867-876

 - Malembic-Maher, S., Salar, P., Filippin, L., Carle, P., Angelini, E. et Foissac, X. 2011. Genetic diversity of European phytoplasmas of the 16SrV taxonomic group and proposal of 'Candidatus Phytoplasma rubi'. International Journal of Systematic and Evolutionary Microbiology,61: 2129-2134.

 - Papura, D., Burban, C., van Helden, M., Giresse, X., Nusillard, B., Guillemaud, T. et Kerdelhue, C. 2012. Microsatellite and mitochondrial data provide evidence for a single major introduction for the neartic leafhopper Scaphoideus titanus in Europe. PLOS ONE, 7: 1-13.

Insect vector identified before the pathogen

The nature of the disease was not initially apparent. One of the earliest theories was that flavescence dorée was the result of root asphyxia. Caudwell then put forward the idea of a yellows disease caused by a virus. Since yellows are transmitted by an animal vector, work was undertaken to discover the vector. The S. titanus leafhopper was then discovered in a Bordeaux vineyard. The pathogen was only identified a number of years later, through an experimental scheme using another leafhopper species and beans as a host plant, once microscope techniques were able to observe the very tiny organisms.