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

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/vmp1Ca. 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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 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 

  2. 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 

  3. 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 

  4. 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 

  5. 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.

  6. 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 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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.

  14. 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 

  15. 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 

  16. 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 

  17. 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 

  18. 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 

  19. 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 

  20. 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 

  21. 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 

  22. 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.

  23. 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 

  24. 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 

  25. 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 

  26. 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 

  27. 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 

  28. 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 

  29. 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 

  30. 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 

  31. 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.

  32. 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 

  33. 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 

  34. 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 

  35. 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 

  36. 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 

  37. 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 

  38. 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 

  39. 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 

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

    Google Scholar 

  41. 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 

  42. 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 

  43. 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 

  44. 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 

  45. 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 

  46. 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 

  47. 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 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

  52. 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 

  53. 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 

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

    Google Scholar 

  55. 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 

  56. 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 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jelena Jović.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

No specific permits were required, as the study did not involve endangered or protected species.

Ethical approval

The authors bear all the ethical responsibilities of this manuscript.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Genetic differentiation
  • Host-plant associations
  • Insect-vector
  • Mitochondrial COI gene marker
  • Multilocus genotyping
  • tuf/stamp/vmp1
  • Stolbur phytoplasma
  • Vector role