Major Outbreaks in the Nineteenth Century Shaped Grape Phylloxera Contemporary Genetic Structure in Europe

Abstract

Grape phylloxera is native to North America, where Vitis spp. acquired different mechanisms of resistance to leaf and root attack. Its appearance in European vineyards at the beginning of the 1860s, where the phylloxera-susceptible grapevine species V. vinifera L. is majorly cultivated, caused the devastation of a great number of vineyards, generating a deep crisis in the European wine production and trade industries. However, the origin and genetic structure of this pest across European vineyards still remain controversial and uncertain. Herein, we analysed the genetic structure of 1173 grape phylloxera individuals collected from 100 locations across eight European countries. Structure and phylogenetic analyses show that contemporary grape phylloxera populations in Europe are the result of at least two independent introductions from the native range that mirrors the historical records that also suggest two major outbreaks in Europe. The comparative analysis with samples from the native range trace back one of these two genetic groups to plants imported from the North East coast of North America, where the American species V. riparia and V. labrusca dominate. This study clarifies the level of genetic diversity of grape phylloxera in Europe and provides relevant information to resolve previous controversy about its origin.

The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

“…Therefore, native populations of the upper Mississippi River region, which feed on the wild riverbank grape (Vitis riparia), could represent the source of the historic invasion of Europe by phylloxera. This result linking European population and V. riparia native populations is consistent with preceding studies using mitochondrial [94] or microsatellite markers [95]. This area, known as French Louisiana in the seventeenth and eighteenth centuries, was under strong French influence and had intense commercial exchanges with France and the rest of Europe into the nineteenth century.…”

Population genetic analysis in old Montenegrin vineyards reveals ancient ways currently active to generate diversity in Vitis vinifera

“…Winemaking practices were partially restored under the rule of Nikola I (1860–1918), which promoted wine exports to Western countries. After several millennia of genetic diversification, most of the grapevine genetic diversity generated in the Balkans was destroyed by the effect of phylloxera and mildews introduced from North America at the end of the nineteenth century 2 , 11 . As a result, many old autochthonous cultivars of the Western Balkans exist now as isolated plants or as relict populations, often represented by few specimens found in old, traditional vineyards or maintained in ex situ Vitis collections 6 , 12 , 13 .…”

“…Winemaking in Montenegro mainly relies on the production of red wine from two autochthonous grape cultivars, Vranac and Kratošija 17 . Kratošija was the dominant variety in the region until the phylloxera crisis, which forced the removal of many old vines and their replacement by new plant material 11 . In many cases, withered Kratošija vines were replaced by grafted Vranac plants, preferred by growers as it produces highly deep-colored wines 17 .…”

Europe as a bridgehead in the worldwide invasion history of grapevine downy mildew,Plasmopara viticola

“…New invasions by additional P. viticola strains or lineages would have a major effect on the wine industry, by destabilizing grapevine protection and canceling out the sustained efforts of breeders to obtain good-quality grapevine varieties resistant to downy mildew. The rich historical records available for grape diseases make these diseases excellent case studies for obtaining fundamental insight into the processes underlying biological invasions, showing that worldwide biological invasions can result from the secondary dispersal of a particularly successful invasive population, as for grape phylloxera (48,51). Our findings show that even pathogens subject to very strong bottlenecks and without admixture as a means of generating diversity can achieve successful invasions worldwide, by retaining an ability to evolve rapidly, and thus to develop new virulence against plant resistance (52-54) and resistance to fungicides (21,55,56).…”