“Bois noir” Vectors and Epidemiology

Michael Maixner JKI, Institute for Plant Protection in Fruit Crops and Viticulture, Geilweilerhof, 76833 Siebeldingen, Germany [email protected]

Abstract—The “bois noir” disease of grapevine (BN) is Control of the predominant dual host plants of vectors associated with ‘Candidatus Phytoplasma solani’ (“stolbur” and ‘Ca. P. solani’ is therefore the mostly applied phytoplasma, 16SrXII-A). This phytoplasma is endemic to practice to reduce population density of vectors and Europe and neighboring regions and infects various wild thereby infection pressure to grapevine. New approaches and cultivated plant species and vectors. Although the aim at the identification of semiochemicals to manipulate principle epidemiology of BN with respect to major host vector’s behavior or the use of potential antagonists of ‘Ca. plants and vectors is long known, detailed knowledge of P. solani’ that might be disseminated by vectors. The the various elements of the pathosystem are still lacking. influence of landscape structure, cultivation practice and Several recent studies aim at the analysis of insect-plant- environmental factors on the vector’s spatiotemporal phytoplasma associations and their consequences for BN epidemiology. This information is not only required for the distribution and migration activity is also analyzed with understanding of BN outbreaks and the cyclic variation of the objective to achieve more specific and effective BN infection pressure, but also a prerequisite for improved management strategies. . management strategies for BN and other diseases of BN is embedded in an intricate pathosystem that economic importance associated with the presence of ‘Ca. P. includes a wide spectrum of host plant species and solani’. This presentation summarizes the progress related to BN epidemiology since the 4th Bois noir workshop in pathogen genotypes together with a range of principal and 2016. minor vector species. Deciphering their interactions does not only contribute to the identification of the drivers of infection pressure to grapevine, but also helps to “Stolbur” phytoplasma is closely associated with understand the reasons of new disease outbreaks and of the family . obsoletus possible future risks. Previous studies revealed that is the principle vector of BN, while Reptalus panzeri acts phenomena like vector’s plant host shift and range as an additional vector in southeast Europe. expansion in combination with the uptake and further Pentastiridius leporinus transmits the phytoplasma to dissemination of ‘Ca. P. solani’ strains in the new host sugar beet, but it is not associated with grapevine. On can lead to new outbreaks of BN. Based on such the other hand, R. quinquecostatus is common on observations, the analysis of the genetic structure of grapevine in some geographic regions, has been vector populations and the variability of ‘Ca. P. solani’ frequently found carrying ‘Candidatus Phytoplasma strains in relation to host plant utilization has developed solani’, and its principal vectoring ability has been to an important field of current investigations. Most demonstrated, but proof of transmission to grapevine is interesting are studies in the presumable center of genetic still lacking. This applies to further Cixiid species of variation of H. obsoletus in south-eastern Europe and Hyalesthes, Reptalus, Cixius and other genera which adjacent regions. The use of non-ribosomal markers for were identified as carriers of ‘Ca. P. solani’. Some multi locus sequence typing of ‘Ca. P. solani’ strains as leafhopper species of the subfamilies Agalliinae and well as mitochondrial and nuclear markers to study H. Deltocephalinae are also able to transmit ‘Ca. P. solani’ obsoletus population genetics provides new insights into to test plants and probably to grapevine, but their the complex pathosystem of “ stolbur” and allows to significance as vectors might be low compared to uncover specific transmission pathways of ‘Ca. P. Cixiidae. It has to be emphasized that the mere detection solani’ from the wild compartment to grapevine. of ‘Ca. P. solani’ in an Auchenorrhyncha species is no Different levels of host adaptation of the principal proof of its ability to transmit it but might initiate vector, ranging from feeding preferences to genetic host further transmission trials. Results suggesting ‘Ca. P. races and presumed cryptic species of H. obsoletus have solani’ detection in extraordinary families of been revealed recently. The role of minor vector species Auchenorrhyncha should be critically scrutinized. There should not been neglected. They might be of marginal is also some confusion regarding host plants of vectors. significance for the direct transmission of ‘Ca. P. solani’ Adults of many species use a wide range of plants for to grapevine and other important crops, but they are feeding, but the term host-plant should be restricted to probably key elements for the pathosystem by species which are confirmed hosts of immature stages. interconnecting otherwise distinct transmission cycles in Management of BN depends in principle on the control the wild compartment. This is indicated by the of vectors, but due to their erratic feeding behavior on detection of ‘Ca. P. solani’ genotypes in minor vector grapevine and their affiliation to the wild vegetation the species that are not known from infected grapevine. direct control by insecticides as it is practiced against “Stolbur” strains transmitted by minor vector species ampelophagous vectors is ineffective. could be picked up by principal vectors with the consequence of new disease outbreaks in major crops.

REFERENCES Kosovac, A., Johannesen, J., Krstic, O., Mitrovic, M., Cvrkovic, T., Tosevski, I., Jovic, J. (2018). Widespread plant specialization in the Papers related to BN vectors and epidemiology polyphagous (Cixiidae), a major th vector of stolbur phytoplasma: evidence of cryptic speciation. PLoS published since the 4 Bois noir workshop at One, 13 (5). doi:ARTN e0196969, 10.1371/journal.pone.0196969 Klosterneuburg, Austria in March 2016. Kosovac, A., Radonjic, S., Hrncic, S., Krstic, O., Tosevski, I., Jovic, J. (2016a). Molecular tracing of the transmission routes of “bois noir” in Mediterranean vineyards of Montenegro and experimental evidence Balakishiyeva, G., Bayramova, J., Mammadov, A., Salar, P., Danet, for the epidemiological role of Vitex agnus-castus (Lamiaceae) J-L., Ember, I., Verdin, E., Foissac, X., Huseynova, I. (2018). and associated Hyalesthes obsoletus (Cixiidae). Plant Pathology, 65 Important genetic diversity of ‘Candidatus Phytoplasma solani’ (2), 285298. related strains associated with bois noir grapevine yellows and planthoppers in Azerbaijan. European Journal of Plant Pathology, Mitrovic, M., Jakovljevic, M., Jovic, J., Krstic, O., Kosovac, A., 151 (4), 937–946. Trivellone, V., Jermini, M., Tosevski, I., Cvrkovic, T. (2016). 'Candidatus Phytoplasma solani' genotypes associated with potato Chuche, J., Danet, J-L., Rivoal, J. B., Arricau-Bouvery, N., Thiery, D. “stolbur” in Serbia and the role of Hyalesthes obsoletus and (2018). Minor cultures as hosts for vectors of extensive crop Reptalus panzeri (, cixiidae) as natural vectors. European diseases: Does Salvia sclarea act as a pathogen and vector Journal of Plant Pathology, 144 (3), 619-630. reservoir for lavender decline? Journal of Pest Science, 91 (1), 145-155. Mori, N., Pozzebon, A., Duso, C., Reggiani, N., Pavan, F. (2016). Vineyard Colonization by Hyalesthes obsoletus (Hemiptera: Chuche, J., Danet, J-L., Salar, P., Foissac, X., Thiery, D. (2016). Cixiidae) induced by stinging nettle cut along surrounding ditches. Transmission of 'Candidatus Phytoplasma solani' by Reptalus Journal of Economic Entomology, 109 (1), 49-56. quinquecostatus (Hemiptera: Cixiidae). Annals of Applied Biology, 169 (2), 214-223. Mori, N., Quaglino, A., Sanna, F., Filisetti, S., Faccincani, M., Bianco, P. A. (2018). Potential role of Euscelis incisus Kirschbaum and Duric, Z., Hrncic, S., Delic, D. (2017). Morphological and Dicranotropis hamata Boheman in the transmission of ‘Candidatus molecular identification of Hyalesthes obsoletus Signoret Phytoplasma solani’ to grapevine. Proceedings of the 19th Congress of (Auchenorrhyncha: Cixiidae) in Herzegovina vineyards. ICVG, Santiago, Chile, April 9-12, 90-91. Mitteilungen Klosterneuburg, 67, 177-181. Panassiti, B., Hartig, F., Fahrentrapp, J., Breuer, M., Biedermann, R. Foissac, X., Jreijiri, F., Salar, P., Wakim, S., Danet, J-L., Choueiri, E. (2017). Identifying local drivers of a vector-pathogen-disease system (2018). A ‘Candidatus Phytoplasma omanense’-related strain using Bayesian modeling. Basic and Applied Ecology, 18, 75-85. detected in yellowing grapevine, stunted bindweed and Cixiidae Pierro, R., Passera, A., Panattoni, A., Casati, P., Luvisi, A., Rizzo, D., planthoppers in Lebanon. European Journal of Plant Pathology, Materazzi, A. (2018). molecular typing of “bois noir” phytoplasma doi:10.1007/s10658- 018-1525-5 strains in the Chianti Classico area (Tuscany, Central Italy) and their Girsova, N. V., Bottner-Parker, K. D., Bogoutdinov, D. Z., Meshkov, association with symptom severity in Vitis vinifera Sangiovese. Y. I., Mozhaeva, K. A., Kastalyeva, T. B., Lee, I-M. (2016). Phytopathology, 108 (3), 362-373. Diverse phytoplasmas associated with potato “stolbur” and Riolo, P., Minuz, R. L., Peri, E., Isidoro, N. (2017). Behavioral responses other related potato diseases in Russia. European Journal of of Hyalesthes obsoletus to host-plant volatiles cues. -Plant Plant Pathology, 145 (1), 139-153. Interactions, 11 (1), 71-78. Hossard, L., Guimier, S., Vinatier, F., Barbier, J. M., Delmotte, S., Trivellone, V., Filippin, L., Narduzzi-Wicht, B., Angelini, E. (2016). A Fontaine, M., Rivoal, J. B. (2018). Source of Hyalesthes regional-scale survey to define the known and potential vectors of obsoletus Signoret planthopper (Hemiptera: Cixiidae) in grapevine yellow phytoplasmas in vineyards South of Swiss Alps. southern France and potential effects of landscape. Bulletin of European Journal of Plant Pathology, 145 (4), 915-927. Entomological Research, 108 (2), 213-222. Zambon, Y., Canel, A., Bertaccini, A., Contaldo, N. (2018). Molecular Iasur-Kruh, L., Naor, V., Zahavi, T., Ballinger, M. J., Sharon, R., diversity of phytoplasmas associated with grapevine yellows disease Robinson, E., Perlman, S. J., Zchori-Fein, E. (2017). Bacterial in north-eastern Italy. Phytopathology, 108 (2), 206-214. associates of Hyalesthes obsoletus (Hemiptera: Cixiidae), the insect vector of bois noir disease, with a focus on cultivable bacteria. Research in Microbiology, 168 (1), 94-101. Iasur-Kruh, L., Zahavi, T., Barkai, R., Freilich, S., Zchori-Fein, E., Naor, W. (2018). Dyella-like bacterium isolated from an insect as a potential biocontrol agent against grapevine yellows. Phytopathology, 108 (3), 336-341.