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European Journal of Plant Pathology

, Volume 151, Issue 4, pp 937–946 | Cite as

Important genetic diversity of ‘Candidatus Phytoplasma solani’ related strains associated with bois noir grapevine yellows and planthoppers in Azerbaijan

  • G. Balakishiyeva
  • J. Bayramova
  • A. Mammadov
  • P. Salar
  • J.-L. Danet
  • I. Ember
  • E. Verdin
  • X. Foissac
  • I. Huseynova
Article

Abstract

Bois noir (BN) is an important grapevine yellows endemic to the Euro-Mediterranean basin caused by ‘Candidatus Phytoplasma solani’ (‘Ca. P. solani’), a non culturable plant pathogenic Mollicute. Bois noir symptoms could be associated with ‘Ca. P. solani’ in two Azerbaijanian vineyards where disease incidence and severity were recorded for five local Vitis vinifera cultivars. In order to gain insight into the epidemiology of Bois noir in Azerbaijan, ‘Ca. P. solani’ isolates infecting plants were characterized by multi-locus sequence analysis and their secY and stamp gene sequences compared to that of the strains detected in other plants and in local Cixiidae planthoppers. Genotypes were determined for two non-ribosomal house-keeping genes, namely tuf and secY, as well as two variable markers namely Stamp and mleP1 genes, that respectively encode the antigenic membrane protein AMP and a 2-Hydroxycarboxylate transporter. The Azerbaijanian BN phytoplasma isolates corresponded to three tufB and secY genotypes. A finer differentiation of Azerbaijanian ‘Ca. P. solani’ isolates was obtained with mleP1 as five different mleP1 genetic variants were found. Finally, Stamp gene allowed differentiating four new genotypes in grapevine among the 10 new Stamp genotypes detected in various plants in Azerbaijan. The preliminary survey for infected insects conducted in northern Azerbaijan, led to the identification of Hyalesthes obsoletus and Reptalus noahi as potential vectors for two ‘Ca. P. solani’ new genotypes phylogenetically distant from the known genetic clusters. Altogether these results indicate an important genetic diversity of BN phytoplasmas in Azerbaijan that certainly result from spread through local insect vectors.

Keywords

Plant pathogen Vitis vinifera Cixiidae MLSA Tuf secY mleP1 Stamp 

Notes

Author contribution

All authors have been personally and actively involved in substantive work leading to the manuscript. Conceived and designed the experiments: GB, XF, IH; Performed the survey: GB, AM, EV, JB, XF. Identified insects: J-LD; Performed the molecular experiments: GB, JB, AM, PS, IE; Analyzed the data: GB, IH, XF; Contributed reagents/materials/analysis tools: IH, XF. Wrote the paper: GB, XF.

Funding

This study was funded by Science Development Foundation under the President of Azerbaijan Republic, Grant № EIF-2013-9(15)-46/28/3) and the INRA meta-programme Sustainable Management of Crop Health SMACH LYCOVITIS.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Human and animal rights

This research does not include any animal and/or human trials.

All sequences have been deposited in the European Nucleotide Archive under the study accession number PRJEB21652.

Supplementary material

10658_2018_1429_MOESM1_ESM.doc (78 kb)
Table S1 Additional sequences used for Stamp phylogenetic analyses (DOC 78 kb)

References

  1. Arnaud, G., Malembic-Maher, S., Salar, P., et al. (2007). Multilocus sequence typing confirms the close genetic interrelatedness of three distinct flavescence doree phytoplasma strain clusters and group 16SrV phytoplasmas infecting grapevine and alder in Europe. Applied and Environmental Microbiology, 73, 4001–4010.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aryan, A., Brader, G., Mörtel, J., Pastar, M., & Riedle-Bauer, M. (2014). An abundant ‘Candidatus Phytoplasma solani’ tuf b strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus. European Journal of Plant Pathology, 140, 213–227.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Atanasova, B., Jakovljević, M., Spasov, D., et al. (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.CrossRefGoogle Scholar
  4. Balakishiyeva, G., Danet, J.-L., Qurbanov, M., Mamedov, A., Kheyr-Pour, A., & Foissac, X. (2010). First report of phytoplasma infections in several temperate fruit trees and vegetable crops in Azerbaijan. Journal of Plant Pathology, 92, 115.Google Scholar
  5. Balakishiyeva, G., Danet, J.-L., Mamedov, A., Huseynova, I. M., & Foissac, X. (2012). Genetic variability of stolbur phytoplasmas in Azerbaijan. Reports of Azerbaijan National Academy of Sciences LXVIII, 2, 66–73.Google Scholar
  6. Balakishiyeva, G., Danet, J.-L., Mammadov, A., Huseynova, I., & Foissac, X. (2013). Survey of ‘Candidatus Phytoplasma solani’ and its potential vectors in Northern regions of Azerbaijan. In E. Torres, A. Lavina, A. Batlle (Eds.), Third European Bois Noir Workshop (pp. 56–58). Barcelona.Google Scholar
  7. Balakishiyeva, G., Mamedov, A., Foissac, X., Huseynova, I., & Aliyev, J. (2016). First report of grapevine ‘bois noir’ in Azerbaijan. Plant Disease, 100, 2522.CrossRefGoogle Scholar
  8. Cimerman, A., Pacifico, D., Salar, P., Marzachi, 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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cimerman, A., Arnaud, G., & Foissac, X. (2006). Stolbur phytoplasma genome survey achieved using a suppression subtractive hybridization approach with high specificity. Applied and Environmental Microbiology, 72, 3274–3283.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Danet, J.-L., Balakishiyeva, G., Cimerman, A., et al. (2011). Multilocus sequence analysis reveals the genetic diversity of European fruit tree phytoplasmas and the existence of inter species recombination. Microbiology, 157, 438–450.CrossRefPubMedGoogle Scholar
  12. Delić, D., Balech, B., Radulović, M., et al. (2016). Vmp1 and Stamp genes variability of ‘Candidatus phytoplasma solani’ in Bosnian and Herzegovinian grapevine. European Journal of Plant Pathology, 145, 221–225.CrossRefGoogle Scholar
  13. Ember, I., Acs, Z., Munyaneza, J. E., et al. (2011). Survey and molecular detection of phytoplasmas associated with potato in Romania and southern Russia. European Journal of Plant Pathology, 130, 367–377.CrossRefGoogle Scholar
  14. Ember, I., Bodor, P., Zsófi, Z., et al. (2016). Impact of bois noir disease on grapevine performance and wine quality. Mitteilungen Klosterneuburg, 66(1), 79–83.Google Scholar
  15. Emeljanov, A. F. (1995). The new taxa of the tribe Pentastirini (Homoptera, Cixiidae) from Palaearctic. Zoologicheskii Zhurnal, 74(9), 73–89.Google Scholar
  16. Ewing, B., Hillier, L., Wendl, M., & Green, P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Research, 8, 175–185.CrossRefPubMedGoogle Scholar
  17. Fabre, A., Danet, J.-L., & Foissac, X. (2011a). The stolbur phytoplasma antigenic membrane protein gene Stamp is submitted to diversifying positive selection. Genes, 472, 37–41.Google Scholar
  18. Fabre, A., Balakishiyeva, G., Ember, I., et al. (2011b). Stamp encoding the antigenic membrane protein of stolbur phytoplasma is useful for molecular epidemiology. Bulletin of Insectology, 64, 21–22.Google Scholar
  19. Fialova, R., Valova, P., Balakishiyeva, G., et al. (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
  20. 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 E. Torres, A. Lavina, A. Batlle (Eds.), Invited conference, Third European Bois Noir Workshop (pp. 11–13). Barcelona.Google Scholar
  21. Foissac, X., Danet, J. L., Zreik, L., et al. (2000). Cloning of the spoT gene of ‘Candidatus Phlomobacter fragariae’ and development of a PCR-restriction fragment length polymorphism assay for detection of the bacterium in insects. Applied and Environmental Microbiology, 66, 3474–3480.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gordon, D. C., Abajian, C., & Green, P. (1998). Consed: A graphical tool for sequence finishing. Genome Research, 8, 195–202.CrossRefPubMedGoogle Scholar
  23. Gundersen, D. E., & Lee, I. M. (1996). Ultrasensitive detection of phytoplasmas by nested-PCR assays using two universal primer pairs. Phytopathologia Mediterranea, 35, 114–151.Google Scholar
  24. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Holzinger, W. E., Kammerlander, I., & Nickel, H. (2003). The Auchenorrhyncha of Central Europe. Die Zikaden Mitteleuropas: 1. Fulgoromorpha, Cicadomorpha excl. Cicadellidae. Leiden: Brill.Google Scholar
  26. Kosovac, A., Radonjić, S., Hrnić, S., et al. (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.CrossRefGoogle Scholar
  27. Kostadinovska, E., Quaglino, F., Mitrev, S., et al. (2014). Multiple gene analyses identify distinct 'Bois noir' phytoplasma genotypes in the republic of Macedonia. Phytopathologia Mediterranea, 53, 300–310.Google Scholar
  28. Laimer, M., Lemaire, O., Herrbach, E., Goldschmidt, V., Minafra, A., Bianco, P., & Wetzel, T. (2009). Resistance to viruses, phytoplasmas and their vectors in the grapevine in europe: a review. Journal of Plant Pathology, 91, 7–23.Google Scholar
  29. 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.Google Scholar
  30. Lee, I. M., Martini, M., Marcone, C., & Zhu, S. F. (2004). Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of 'Candidatus Phytoplasma ulmi' for the phytoplasma associated with elm yellows. International Journal of Systematic and Evolutionary Microbiology, 54, 337–347.CrossRefPubMedGoogle Scholar
  31. Maixner, M. (1994). Transmission of German grapevine yellows (Vergilbungskrankheit) by the planthopper Hyalesthes obsoletus (Auchenorrhyncha: Cixiidae). Vitis, 33, 103–104.Google Scholar
  32. Maixner, M., Ahrens, U., & Seemuller, E. (1995). Detection of the German grapevine yellows (Vergilbungskrankheit) MLO in grapevine, alternative hosts and a vector by a specific PCR procedure. European Journal of Plant Pathology, 101, 241–250.CrossRefGoogle Scholar
  33. Pacifico, D., Alma, A., Bagnoli, B., et al. (2009). Characterization of bois noir isolates by restriction fragment length polymorphism of a Stolbur-specific putative membrane protein gene. Phytopathology, 99, 711–715.CrossRefPubMedGoogle Scholar
  34. Quaglino, F., Zhao, Y., Casati, P., et al. (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.CrossRefPubMedGoogle Scholar
  35. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • G. Balakishiyeva
    • 1
  • J. Bayramova
    • 1
  • A. Mammadov
    • 1
  • P. Salar
    • 2
  • J.-L. Danet
    • 2
  • I. Ember
    • 4
    • 5
  • E. Verdin
    • 3
  • X. Foissac
    • 2
  • I. Huseynova
    • 1
  1. 1.Institute of Molecular Biology and BiotechnologyAzerbaijan National Academy of SciencesBakuAzerbaijan
  2. 2.UMR1332 Biologie du Fruit et Pathologie, INRAUniversité de BordeauxVillenave d’OrnonFrance
  3. 3.UR0407 Unité de Recherche de Pathologie Végétale, INRAMontfavetFrance
  4. 4.Faculty of Horticultural Science, Department of ViticultureSzent István UniversityBudapestHungary
  5. 5.Budapest University of Technology and EconomicsBudapestHungary

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