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Role of plant-specialized Hyalesthes obsoletus associated with Convolvulus arvensis and Crepis foetida in the transmission of ‘Candidatus Phytoplasma solani’-inflicted bois noir disease of grapevine in Serbia

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Abstract

Bois noir (BN), a grapevine yellows disease induced by ‘Candidatus Phytoplasma solani’, is spreading and diversifying in several wine-producing regions of Europe, causing increased yield losses and economic concerns. The planthopper Hyalesthes obsoletus (Hemiptera: Cixiidae) is a major vector of the pathogen that causes BN disease in grapevine. Recent studies suggest that epidemiology of BN is affected by the interaction of specific host races of H. obsoletus with weedy host plants that serve as reservoirs for the pathogen. Since BN is common in grape-growing regions of Serbia, a survey was conducted during 2015–2016 to evaluate the host-plant association and vector role of H. obsoletus in central and eastern regions. We tested populations of H. obsoletus associated with Convolvulus arvensis (field bindweed) a known host for the vector and pathogen and Crepis foetida (stinking hawk’s-beard) a newly identified host in southeastern Europe. Molecular phylogenetic analyses of H. obsoletus collected from C. arvensis and C. foetida using the mtDNA COI marker determined that the two populations had a genetic divergence of 1.4%. Transmission trials confirmed the vector role of C. arvensis-associated H. obsoletus and identified C. foetida-associated populations as a new and efficient host-specialized vector of BN. Each of the two host-specialized vector populations transmitted ‘Ca. P. solani’ to its original host (C. arvensis or C. foetida) and to grapevine cv. Chardonnay. Multilocus genotyping of the transmitted phytoplasma isolates based on tuf/stamp/vmp1 ‘Ca. P. solani’-specific loci indicated pathogen segregation according to the host-plant association of the vector. All isolates transmitted by C. foetida-associated H. obsoletus were of the STOL genotype (tuf-b/STOL/V2-TA), while the C. arvensis-associated population transmitted several genotypes: tuf-b/Rqg50/V4, tuf-b/Rqg50/V14, tuf-b/Rqg31/V14 and tuf-b/Vv24/V14. This study provides evidence of a new independent BN epidemiological cycle of tuf-b ‘Ca. P. solani’ strain in the Balkan region, sourced by C. foetida and transmitted by its associated H. obsoletus population.

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References

  • Aleksić, Ž., Šutić, D., & Aleksić, D. (1967). Transmission intensity of stolbur virus by means of Hyalesthes obsoletus sign. on some host plants. Plant Protection, 93–95, 67–73.

    Google Scholar 

  • Angelini, E., Clair, D., Borgo, M., Bertaccini, A., & Boudon-Padieu, E. (2001). Flavescence dorée in France and Italy – occurrence of closely related phytoplasma isolates and their near relationships to palatinate grapevine yellows and an alder yellows phytoplasma. Vitis, 40, 79–86.

    CAS  Google Scholar 

  • Aryan, A., Brader, G., Mörtel, J., Pastar, M., & Riedle-Bauer, M. (2014). An abundant 'Candidatus Phytoplasma solani' Stolbur tuf b phytoplasma strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus. European Journal of Plant Pathology, 140, 213–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atanasova, B., Jakovljević, M., Spasov, D., Jović, J., Mitrović, M., Toševski, I., & Cvrković, T. (2015). The molecular epidemiology of bois noir grapevine yellows caused by ‘Candidatus Phytoplasma solani’in the Republic of Macedonia. European Journal of Plant Pathology, 142, 759–770.

    Article  Google Scholar 

  • Balakishiyeva, G., Bayramova, J., Mammadov, A., Salar, P., Danet, J.-L., Ember, I., Verdin, E., Foissac, X., & Huseynova, I. (2018). Important genetic diversity of ‘Candidatus Phytoplasma solani’ related strains associated with bois noir grapevine yellows and planthoppers in Azerbaijan. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-018-1429-4.

  • Bertin, S., Picciau, L., Ács, Z., Alma, A., & Bosco, D. (2010). Molecular identification of the Hyalesthes species (Hemiptera: Cixiidae) occurring in vineyard agroecosystems. Annals of Applied Biology, 157, 435–445.

    Article  CAS  Google Scholar 

  • Bressan, A., Holzinger, W. E., Nusillard, B., Sémétey, O., Gatineau, F., Simonato, M., & Boudon-Padieu, E. (2009). Identification and biological traits of a planthopper from the genus Pentastiridius (Hemiptera: Cixiidae) adapted to an annual cropping rotation. European Journal of Entomology, 106(3), 405–413.

    Article  CAS  Google Scholar 

  • Chuche, J., Danet, J. L., Salar, P., Foissac, X., & Thiéry, D. (2016). Transmission of ‘Candidatus Phytoplasma solani’ by Reptalus quinquecostatus (Hemiptera: Cixiidae). Annals of Applied Biology, 169, 214–223.

    Article  Google Scholar 

  • Chuche, J., Danet, J. L., Rivoal, J. B., Arricau-Bouvery, N., & Thiéry, D. (2018). Minor cultures as hosts for vectors of extensive crop diseases: does Salvia sclarea act as a pathogen and vector reservoir for lavender decline? Journal of Pest Science, 91, 145–155.

    Article  Google Scholar 

  • Cimerman, A., Pacifico, D., Salar, P., Marzachì, C., & Foissac, X. (2009). Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the stolbur phytoplasma. Applied and Environmental Microbiology, 75, 2951–2957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clair, D., Larrue, J., Aubert, G., Gillet, J., Cloquemin, G., & Boudon-Padieu, E. (2003). A multiplex nested-PCR assay for sensitive and simultaneous detection and direct identification of phytoplasma in the elm yellows group and Stolbur group and its use in survey of grapevine yellows in France. Vitis, 42, 151–157.

    CAS  Google Scholar 

  • Clement, M., Posada, D., & Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.

    Article  CAS  PubMed  Google Scholar 

  • Cvrković, T. (2010). Diversity of Auchenorrhyncha species in Serbian vineyards and their role in Bois noir transmission. PhD Dissertation, University of Belgrade, Serbia, 120 pp.

  • Cvrković, T., Jović, J., Mitrović, M., Krstić, O., Krnjajić, S., & Toševski, I. (2011). Potential new hemipteran vectors of stolbur phytoplasma in Serbian vineyards. Bulletin of Insectology, 64(Supplement), 129–130.

    Google Scholar 

  • Cvrković, T., Jović, J., Mitrović, M., Krstić, O., & Toševski, I. (2014). Experimental and molecular evidence of Reptalus panzeri as a natural vector of bois noir. Plant Pathology, 63, 42–53.

    Article  CAS  Google Scholar 

  • Daire, X., Clair, D., Reinert, W., & Boudon-Padieu, E. (1997). Detection and differentiation of grapevine yellows phytoplasmas belonging to the elm yellows group and to the stolbur subgroup by PCR amplification of non-ribosomal DNA. European Journal of Plant Pathology, 103, 507–514.

    Article  CAS  Google Scholar 

  • Delić, D., Balech, B., Radulović, M., Lolić, B., Karačić, A., Vukosavljević, V., Đurić, G., & Jovanović Cvetković, T. (2016). Vmp1 and stamp genes variability of ‘Candidatus phytoplasma solani’ in Bosnian and Herzegovinian grapevine. European Journal of Plant Pathology, 145, 221–225.

    Article  CAS  Google Scholar 

  • Duduk, B., Botti, S., Ivanović, M., Krstić, B., Dukić, N., & Bertaccini, A. (2004). Identification of phytoplasmas associated with grapevine yellows in Serbia. Journal of Phytopathology, 152, 575–579.

    Article  CAS  Google Scholar 

  • Đurić, Z., Hrnčić, S., & Delić, D. (2017). Morphological and molecular identification of Hyalesthes obsoletus Signoret (Auchenorrhyncha: Cixiidae) in Herzegovina vineyards. Mitteilungen Klosterneuburg, 67, 177–181.

    Google Scholar 

  • Fabre, A., Danet, J.-L., & Foissac, X. (2011). The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene, 472, 37–41.

    Article  CAS  PubMed  Google Scholar 

  • Fialová, R., Válová, P., Balakishiyeva, G., Danet, J.-L., Šafárová, D., Foissac, X., & Navrátil, M. (2009). Genetic variability of stolbur phytoplasma in annual crop and wild plant species in South Moravia (Czech Republic). Journal of Plant Pathology, 91, 411–416.

    Google Scholar 

  • Foissac, X., Carle, P., Fabre, A., Salar, P., Danet, J. L., & STOLBUR-EUROMED consortium. (2013). ‘Candidatus Phytoplasma solani’ genome project and genetic diversity in the Euro-Mediterranean basin. In: Torres, E., Lavina, A., & Batlle, A., eds. Proceedings of 3rd European Bois Noir Workshop (pp. 11–13). Barcelona, Spain.

  • Güclü, S., & Ozbek, H. (1988). Some studies on the biology of Hyalesthes obsoletus Signoret (Homoptera: Cixidae) in the conditions of Erzurum. Turkiye Entomoloji Dergisi, 12, 103–111.

    Google Scholar 

  • Hoch, H., & Remane, R. (1985). Evolution und Speziation der Zikaden-Gattung Hyalesthes SIGNORET, 1865 (Homoptera Auchenorrhyncha Fulgoroidea Cixiidae). Marburger Entomologische Publikationen, 2, 1–427.

    Google Scholar 

  • Horváth, G. (1891). Hemipterološki izlet u Primorje i Plitvička jezera. Glasnik Hrvatskoga Naravoslovnoga Drustva (Societas historico-naturalis Croatica), VI(1–5), 29–49.

    Google Scholar 

  • Imo, M., Maixner, M., & Johannesen, J. (2013). Sympatric diversification vs. immigration: deciphering host-plant specialization in a polyphagous insect, the stolbur phytoplasma vector Hyalesthes obsoletus (Cixiidae). Molecular Ecology, 22, 2188–2203.

    Article  PubMed  Google Scholar 

  • Johannesen, J., & Riedle-Bauer, M. (2014). Origin of a sudden mass occurrence of the stolbur phytoplasma vector Hyalesthes obsoletus (Cixiidae) in Austria. Annals of Applied Biology, 165, 488–495.

    Article  Google Scholar 

  • Johannesen, J., Lux, B., Michel, K., Seitz, A., & Maixner, M. (2008). Invasion biology and host specificity of the grapevine yellows disease vector Hyalesthes obsoletus in Europe. Entomologia Experimentalis et Applicata, 126, 217–227.

    Article  CAS  Google Scholar 

  • Johannesen, J., Foissac, X., Kehrli, P., & Maixner, M. (2012). Impact of vector dispersal and host-plant fidelity on the dissemination of an emerging plant pathogen. PLoS One, 7, e51809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kessler, S., Schaerer, S., Delabays, N., Turlings, T. C., Trivellone, V., & Kehrli, P. (2011). Host plant preferences of Hyalesthes obsoletus, the vector of the grapevine yellows disease ‘bois noir’, in Switzerland. Entomologia Experimentalis et Applicata, 139, 60–67.

    Article  Google Scholar 

  • Kosovac, A., Johannesen, J., Krstić, O., Mitrović, M., Cvrković, T., Maixner, M., Toševski, I., & Jović, J. (2013). Microsatellite and mtDNA evidence of genetic differentiation in Hyalesthes obsoletus populations associated with a new major host, stinking hawk’s-beard (Crepis foetida), in southeast Europe. In: Torres, E., Lavina, A., & Batlle, A., eds. Proceedings of 3rd European Bois Noir Workshop (pp. 18–19). Barcelona, Spain.

  • Kosovac, A., Jakovljević, M., Krstić, O., Cvrković, T., Mitrović, M., Toševski, I., & Jović, J. (2014). Crepis foetida L.: new host plant of cixiid planthopper Hyalesthes obsoletus Signoret 1865 (Hemiptera: Cixiidae), vector of stolbur phytoplasma. Plant Protection, 65, 7–14.

    Article  Google Scholar 

  • Kosovac, A., Radonjić, S., Hrnčić, S., Krstić, O., Toševski, I., & Jović, J. (2016). Molecular tracing of the transmission routes of bois noir in Mediterranean vineyards of Montenegro and experimental evidence for the epidemiological role of Vitex agnus-castus (Lamiaceae) and associated Hyalesthes obsoletus (Cixiidae). Plant Pathology, 65, 285–298.

    Article  CAS  Google Scholar 

  • Kosovac, A., Johannesen, J., Krstić, O., Mitrović, M., Cvrković, T., Toševski, I., & Jović, J. (2018). Widespread plant specialization in the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), a major vector of stolbur phytoplasma: evidence of cryptic speciation. PLoS One, 13(5), e0196969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krstić, O., Cvrković, T., Mitrović, M., Radonjić, S., Hrnčić, S., Toševski, I., & Jović, J. (2018). Wolbachia infection in natural populations of Dictyophara europaea, an alternative vector of grapevine Flavescence dorée phytoplasma: effects and interactions. Annals of Applied Biology, 172, 47–64.

    Article  CAS  Google Scholar 

  • Kuzmanović, S., Martini, M., Ermacora, P., Ferrini, F., Starović, M., Tosić, M., Carraro, L., & Osler, R. (2008). Incidence and molecular characterization of Flavescence dorée and stolbur phytoplasmas in grapevine cultivars from different viticultural areas of Serbia. Vitis, 47, 105–111.

    Google Scholar 

  • Langer, M., & Maixner, M. (2004). Molecular characterisation of grapevine yellows associated phytoplasmas of the stolbur group based on RFLP analysis of non-ribosomal DNA. Vitis, 43, 191–199.

    CAS  Google Scholar 

  • Lunt, D. H., Zhang, D. X., Szymura, J. M., & Hewltt, O. M. (1996). The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology, 5, 153–165.

    Article  CAS  PubMed  Google Scholar 

  • Mahuku, G. S. (2004). A simple extraction method suitable for PCR-based analysis of plant, fungal, and bacterial DNA. Plant Molecular Biology Reporter, 22, 71–81.

    Article  CAS  Google Scholar 

  • Maixner, M. (1994). Transmission of German grapevine yellows (Vergilbungskrankheit) by the planthopper Hyalesthes obsoletus (Auchenorrhyncha: Cixiidae). Vitis, 33, 103–104.

    Google Scholar 

  • Maniyar, B., Kehrli, P., & Johannesen, J. (2013). Population structure and incidence of the stolbur phytoplasma vector Hyalesthes obsoletus (Cixiidae) among geographic regions in Switzerland. Journal of Applied Entomology, 137, 589–600.

    Article  Google Scholar 

  • Mitrović, M., Jakovljević, M., Jović, J., Krstić, O., Kosovac, A., Trivellone, V., Jermini, M., Toševski, I., & Cvrković, T. (2016). 'Candidatus Phytoplasma solani' genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (Hemiptera, Cixiidae) as natural vectors. European Journal of Plant Pathology, 144, 619–630.

    Article  Google Scholar 

  • Pinzauti, F., Trivellone, V., & Bagnoli, B. (2008). Ability of Reptalus quinquecostatus (Hemiptera: Cixiidae) to inoculate stolbur phytoplasma to artificial feeding medium. Annals of Applied Biology, 153, 299–305.

    Article  Google Scholar 

  • Quaglino, F., Zhao, Y., Casati, P., Bulgari, D., Bianco, P. A., Wei, W., & Davis, R. E. (2013). ‘Candidatus Phytoplasma solani’, a novel taxon associated with stolbur- and bois noir-related diseases of plants. International Journal of Systematic and Evolutionary Microbiology, 63, 2879–2894.

    Article  CAS  PubMed  Google Scholar 

  • Quaglino, F., Maghradze, D., Casati, P., Chkhaidze, N., Lobjanidze, M., Ravasio, A., Passera, A., Venturini, G., Failla, O., & Bianco, P. A. (2016). Identification and characterization of new ‘Candidatus Phytoplasma solani’ strains associated with bois noir disease in Vitis vinifera L. cultivars showing a range of symptom severity in Georgia, the Caucasus region. Plant Disease, 100, 904–915.

    Article  CAS  PubMed  Google Scholar 

  • Radonjić, S., Hrnčić, S., Jović, J., Cvrković, T., Krstić, O., Krnjajić, S., & Toševski, I. (2009). Occurrence and distribution of grapevine yellows caused by stolbur phytoplasma in Montenegro. Journal of Phytopathology, 157, 682–685.

    Article  Google Scholar 

  • Rees, D. J., Emerson, B. C., Oromi, P., & Hewitt, G. M. (2001). Mitochondrial DNA, ecology and morphology: interpreting the phylogeography of the Nesotes (Coleoptera: Tenebrionidae) of gran Canaria (Canary Islands). Molecular Ecology, 10, 427–434.

    Article  CAS  PubMed  Google Scholar 

  • Riedle-Bauer, M., Sára, A., & Regner, F. (2008). Transmission of a stolbur phytoplasma by the agalliinae leafhopper Anaceratagallia ribauti (Hemiptera, Auchenorrhyncha, Cicadellidae). Journal of Phytopathology, 156, 687–690.

    Article  Google Scholar 

  • Sforza, R., Clair, D., Daire, X., Larrue, J., & Boudon-Padieu, E. (1998). The role of Hyalesthes obsoletus (Hemiptera: Cixiidae) in the occurrence of bois noir of grapevines in France. Journal of Phytopathology, 146, 549–556.

    Article  Google Scholar 

  • Sforza, R., Bourgoin, T., Wilson, S. W., & Boudon-Padieu, E. (1999). Field observations, laboratory rearing and descriptions of immatures of the planthopper Hyalesthes obsoletus (Hemiptera: Cixiidae). European Journal of Entomology, 96, 409–418.

    Google Scholar 

  • Sharon, R., Soroker, V., Wesley, S. D., Zahavi, T., Harari, A., & Weintraub, P. G. (2005). Vitex agnus-castus is a preferred host plant for Hyalesthes obsoletus. Journal of Chemical Ecology, 31, 1051–1063.

    Article  CAS  PubMed  Google Scholar 

  • Sharon, R., Harari, A. R., Zahavi, T., Raz, R., Dafny-Yelin, M., Tomer, M., Sofer-Arad, C., Weintraub, P. G., & Naor, V. (2015). A yellows disease system with differing principal host plants for the obligatory pathogen and its vector. Plant Pathology, 64, 785–791.

    Article  Google Scholar 

  • Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., & Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87, 651–701.

    Article  CAS  Google Scholar 

  • Swofford, D. L. (2002). PAUP* phylogenetic analysis using parsimony (*and other methods). Sunderland: Sinauer Associates.

    Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was funded by Ministry of Education, Science and Technological Development of the Republic of Serbia (III43001) and partly by the SCOPES program of the Swiss National Science Foundation (IZ73Z0_152414). The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Plant Pests, Institute for Plant Protection and Environment, Banatska 33, Zemun, 11080, Serbia

    Andrea Kosovac, Miljana Jakovljević, Oliver Krstić, Tatjana Cvrković, Milana Mitrović, Ivo Toševski & Jelena Jović

  2. CABI, 1 Rue des Grillons, 2800, Delémont, Switzerland

    Ivo Toševski

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  1. Andrea Kosovac
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Kosovac, A., Jakovljević, M., Krstić, O. et al. Role of plant-specialized Hyalesthes obsoletus associated with Convolvulus arvensis and Crepis foetida in the transmission of ‘Candidatus Phytoplasma solani’-inflicted bois noir disease of grapevine in Serbia. Eur J Plant Pathol 153, 183–195 (2019). https://doi.org/10.1007/s10658-018-1553-1

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