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When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence dorée epidemics in Europe

Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Malembic-Maher, Sylvie;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Desqué, Delphine;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Khalil, Dima;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Salar, Pascal;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Bergey, Bernard;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Danet, Jean-Luc;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Duret, Sybille;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Dubrana-Ourabah, Marie-Pierre;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Beven, Laure;
Affiliation
Genlogs Biodiagnosztika Ltd, Hungary
Ember, Ibolya;
Affiliation
Genlogs Biodiagnosztika Ltd, Hungary
Acs, Zoltan;
Affiliation
Department of Agriculture, Food and Environment, University of Pisa, Italy
Bartola, Michele Della;
Affiliation
Department of Agriculture, Food and Environment, University of Pisa, Italy
Materazzi, Alberto;
Affiliation
CREA Viticulture and Enology, Conegliano (TV), Italy
Filippin, Luisa;
Affiliation
Department of Plant Pests, Institute of Plant Protection and Environment, Zemun, Serbia
Krnjajic, Slobodan;
Affiliation
Department of Plant Pests, Institute of Plant Protection and Environment, Zemun, Serbia
Krstić, Oliver;
Affiliation
Department of Plant Pests, Institute of Plant Protection and Environment, Zemun, Serbia
Toševski, Ivo;
GND
1178357759
Affiliation
Julius Kühn-Institute (JKI), Institute for Plant Protection in Fruit Crops and Viticulture, Germany
Lang, Friederike;
GND
1173192255
Affiliation
Julius Kühn-Institute (JKI), Institute for Plant Protection in Fruit Crops and Viticulture, Germany
Jarausch, Barbara;
Affiliation
Genlogs Biodiagnosztika Ltd, Hungary
Kölber, Maria;
Affiliation
Department of Plant Pests, Institute of Plant Protection and Environment, Zemun, Serbia
Jović, Jelena;
Affiliation
CREA Viticulture and Enology, Conegliano (TV), Italy
Angelini, Elisa;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Arricau-Bouvery, Nathalie;
GND
1059140373
Affiliation
Julius Kühn-Institute (JKI), Institute for Plant Protection in Fruit Crops and Viticulture, Germany
Maixner, Michael;
Affiliation
INRAE, Univ. Bordeaux, UMR BFP, Villenave d'Ornon, France
Foissac, Xavier

Flavescence dorée (FD) is a European quarantine grapevine disease transmitted by the Deltocephalinae leafhopper Scaphoideus titanus. Whereas this vector had been introduced from North America, the possible European origin of FD phytoplasma needed to be challenged and correlated with ecological and genetic drivers of FD emergence. For that purpose, a survey of genetic diversity of these phytoplasmas in grapevines, S. titanus, black alders, alder leafhoppers and clematis were conducted in five European countries. Out of 132 map genotypes, only 11 were associated to FD outbreaks, three were detected in clematis, whereas 127 were detected in alder trees, alder leafhoppers or in grapevines out of FD outbreaks. Most of the alder trees were found infected, including 8% with FD genotypes M6, M38 and M50, also present in alders neighboring FD-free vineyards and vineyard-free areas. The Macropsinae Oncopsis alni could transmit genotypes unable to achieve transmission by S. titanus, while the Deltocephalinae Allygus spp. and Orientus ishidae transmitted M38 and M50 that proved to be compatible with S. titanus. Variability of vmpA and vmpB adhesin-like genes clearly discriminated 3 genetic clusters. Cluster Vmp-I grouped genotypes only transmitted by O. alni, while clusters Vmp-II and -III grouped genotypes transmitted by Deltocephalinae leafhoppers. Interestingly, adhesin repeated domains evolved independently in cluster Vmp-I, whereas in clusters Vmp-II and-III showed recent duplications. Latex beads coated with various ratio of VmpA of clusters II and I, showed that cluster II VmpA promoted enhanced adhesion to the Deltocephalinae Euscelidius variegatus epithelial cells and were better retained in both E. variegatus and S. titanus midguts. Our data demonstrate that most FD phytoplasmas are endemic to European alders. Their emergence as grapevine epidemic pathogens appeared restricted to some genetic variants pre-existing in alders, whose compatibility to S. titanus correlates with different vmp gene sequences and VmpA binding properties.

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License Holder: 2020 Malembic-Maher et al.

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