When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe
2020
Authors
Malembic-Maher, SylvieDesque, Delphine
Khalil, Dima
Salar, Pascal
Bergey, Bernard
Danet, Jean-Luc
Duret, Sybille
Dubrana-Ourabah, Marie-Pierre
Beven, Laure
Ember, Ibolya
Acs, Zoltan
Della, Bartola, Michele
Materazzi, Alberto
Filippin, Luisa
Krnjajić, Slobodan
Krstic, Oliver
Tosevski, Ivo
Lang, Friederike
Jarausch, Barbara
Kolber, Maria
Jović, Jelena
Angelini, Elisa
Arricau-Bouvery, Nathalie
Maixner, Michael
Foissac, Xavier
Article (Published version)
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Author summary Since the first outbreaks, Flavescence doree epidemics had been associated to the introduction of the North American leafhopper vector Scaphoideus titanus. We hereby show that the associated phytoplasma originated from European alders and that epidemics in grapevine are restricted to some phytoplasma genetic variants pre-existing in this wild asymptomatic plant host. The compatibility of this phytoplasma to the introduced S. titanus insect vector resulted from the adaptation of phytoplasma variable membrane proteins Vmps to leafhoppers of the same subfamily living on alders. Vmps organization is similar to adhesion related proteins (ARP) and seems to allow the duplication of pre-adapted repeated domains. This suggests a key role of the Vmp adhesins in the life-style of phytoplasmas infecting woody hosts that rely on the adaptation to new insect vectors to expand their plant-host range. Flavescence doree (FD) is a European quarantine grapevine disease transmitted by the D...eltocephalinae 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.
Keywords:
Flavescence doree / Scaphoideus titanus / Clematis vitalba / insect vector / quarantine disease / genetic diversity / vmp gene sequencesSource:
Plos Pathogens, 2020, 16, 3Publisher:
- Public Library Science, San Francisco
Funding / projects:
- European South Eastern European SEE-ERANET Balkan Initiative network "Global epidemiology of phytoplasma diseases of economic importance in Southeast Europe" grant [06-100003110724]
- Interprofessional Council of Bordeaux' Wine (CIVB) grants [28299, 41044, 6099]
- INRAE Department of Plant Health and Environment (SPE) grant
- Interprofessional Bureau of Burgundy Wines (BIVB) grant [FD-ORIGIN1, FD-ORIGIN2]
- INRA Metaprogramme Sustainable Management of Crop Health (SMACH) grant
- Bilateral French - Hungarian intergovernmental ST program [TET_11_FR-VINEPHYT-HU]
- bilateral French - Hungarian intergovernmental PHC BALATON grant [27853]
- Bilateral French - Serbian intergovernmental PAVLE-SLAVIC grant [23624PG]
- German Academic Exchange Service in the frame of the French-German bilateral exchange program, PROCOPE [57049025]
- European COST action [FA0807, COST-STSM-FA0807-7468, COST-STSMFA0807-05285]
- Modulation of antioxidative metabolism in plants for improvement of plant abiotic stress tolerance and identification of new biomarkers for application in remediation and monitoring of degraded biotopes (RS-MESTD-Integrated and Interdisciplinary Research (IIR or III)-43010)
DOI: 10.1371/journal.ppat.1007967
ISSN: 1553-7366
PubMed: 32210479
WoS: 000523706200019
Scopus: 2-s2.0-85082810210
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Institution/Community
Institut za multidisciplinarna istraživanjaTY - JOUR AU - Malembic-Maher, Sylvie AU - Desque, Delphine AU - Khalil, Dima AU - Salar, Pascal AU - Bergey, Bernard AU - Danet, Jean-Luc AU - Duret, Sybille AU - Dubrana-Ourabah, Marie-Pierre AU - Beven, Laure AU - Ember, Ibolya AU - Acs, Zoltan AU - Della, Bartola, Michele AU - Materazzi, Alberto AU - Filippin, Luisa AU - Krnjajić, Slobodan AU - Krstic, Oliver AU - Tosevski, Ivo AU - Lang, Friederike AU - Jarausch, Barbara AU - Kolber, Maria AU - Jović, Jelena AU - Angelini, Elisa AU - Arricau-Bouvery, Nathalie AU - Maixner, Michael AU - Foissac, Xavier PY - 2020 UR - http://rimsi.imsi.bg.ac.rs/handle/123456789/1389 AB - Author summary Since the first outbreaks, Flavescence doree epidemics had been associated to the introduction of the North American leafhopper vector Scaphoideus titanus. We hereby show that the associated phytoplasma originated from European alders and that epidemics in grapevine are restricted to some phytoplasma genetic variants pre-existing in this wild asymptomatic plant host. The compatibility of this phytoplasma to the introduced S. titanus insect vector resulted from the adaptation of phytoplasma variable membrane proteins Vmps to leafhoppers of the same subfamily living on alders. Vmps organization is similar to adhesion related proteins (ARP) and seems to allow the duplication of pre-adapted repeated domains. This suggests a key role of the Vmp adhesins in the life-style of phytoplasmas infecting woody hosts that rely on the adaptation to new insect vectors to expand their plant-host range. Flavescence doree (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. PB - Public Library Science, San Francisco T2 - Plos Pathogens T1 - When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe IS - 3 VL - 16 DO - 10.1371/journal.ppat.1007967 ER -
@article{ author = "Malembic-Maher, Sylvie and Desque, Delphine and Khalil, Dima and Salar, Pascal and Bergey, Bernard and Danet, Jean-Luc and Duret, Sybille and Dubrana-Ourabah, Marie-Pierre and Beven, Laure and Ember, Ibolya and Acs, Zoltan and Della, Bartola, Michele and Materazzi, Alberto and Filippin, Luisa and Krnjajić, Slobodan and Krstic, Oliver and Tosevski, Ivo and Lang, Friederike and Jarausch, Barbara and Kolber, Maria and Jović, Jelena and Angelini, Elisa and Arricau-Bouvery, Nathalie and Maixner, Michael and Foissac, Xavier", year = "2020", abstract = "Author summary Since the first outbreaks, Flavescence doree epidemics had been associated to the introduction of the North American leafhopper vector Scaphoideus titanus. We hereby show that the associated phytoplasma originated from European alders and that epidemics in grapevine are restricted to some phytoplasma genetic variants pre-existing in this wild asymptomatic plant host. The compatibility of this phytoplasma to the introduced S. titanus insect vector resulted from the adaptation of phytoplasma variable membrane proteins Vmps to leafhoppers of the same subfamily living on alders. Vmps organization is similar to adhesion related proteins (ARP) and seems to allow the duplication of pre-adapted repeated domains. This suggests a key role of the Vmp adhesins in the life-style of phytoplasmas infecting woody hosts that rely on the adaptation to new insect vectors to expand their plant-host range. Flavescence doree (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.", publisher = "Public Library Science, San Francisco", journal = "Plos Pathogens", title = "When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe", number = "3", volume = "16", doi = "10.1371/journal.ppat.1007967" }
Malembic-Maher, S., Desque, D., Khalil, D., Salar, P., Bergey, B., Danet, J., Duret, S., Dubrana-Ourabah, M., Beven, L., Ember, I., Acs, Z., Della, B. M., Materazzi, A., Filippin, L., Krnjajić, S., Krstic, O., Tosevski, I., Lang, F., Jarausch, B., Kolber, M., Jović, J., Angelini, E., Arricau-Bouvery, N., Maixner, M.,& Foissac, X.. (2020). When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe. in Plos Pathogens Public Library Science, San Francisco., 16(3). https://doi.org/10.1371/journal.ppat.1007967
Malembic-Maher S, Desque D, Khalil D, Salar P, Bergey B, Danet J, Duret S, Dubrana-Ourabah M, Beven L, Ember I, Acs Z, Della BM, Materazzi A, Filippin L, Krnjajić S, Krstic O, Tosevski I, Lang F, Jarausch B, Kolber M, Jović J, Angelini E, Arricau-Bouvery N, Maixner M, Foissac X. When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe. in Plos Pathogens. 2020;16(3). doi:10.1371/journal.ppat.1007967 .
Malembic-Maher, Sylvie, Desque, Delphine, Khalil, Dima, Salar, Pascal, Bergey, Bernard, Danet, Jean-Luc, Duret, Sybille, Dubrana-Ourabah, Marie-Pierre, Beven, Laure, Ember, Ibolya, Acs, Zoltan, Della, Bartola, Michele, Materazzi, Alberto, Filippin, Luisa, Krnjajić, Slobodan, Krstic, Oliver, Tosevski, Ivo, Lang, Friederike, Jarausch, Barbara, Kolber, Maria, Jović, Jelena, Angelini, Elisa, Arricau-Bouvery, Nathalie, Maixner, Michael, Foissac, Xavier, "When a Palearctic bacterium meets a Nearctic insect vector: Genetic and ecological insights into the emergence of the grapevine Flavescence doree epidemics in Europe" in Plos Pathogens, 16, no. 3 (2020), https://doi.org/10.1371/journal.ppat.1007967 . .