Epidemiological Role of Dictyophara europaea (Hemiptera: Dictyopharidae) in the Transmission of ‘Candidatus Phytoplasma solani’

Bois noir, an economically important disease of grapevine yellows that causes significant economic losses in wine production, is associated with ‘Candidatus Phytoplasma solani’ and transmitted to grapevines by cixiids Hyalesthes obsoletus and Reptalus panzeri. Polyphagous planthopper Dictyophara europaea, commonly found in natural habitats, harbors phytoplasmas from distinct groups and is an alternative vector in the open epidemiological cycles of the Flavescence dorée phytoplasma in grapevine in European vineyards. This study addresses the role of D. europaea in the transmission cycle(s) of ‘Ca. P. solani’ among wild habitats, natural reservoir plants, and the vineyard agroecosystem using MLSA and transmission trials with naturally infected adults to grapevine and Catharanthus roseus. The infection rates of D. europaea ranged from 7% to 13% in diverse locations, while reservoir herbaceous plants were infected in the amount of 29%. A total of 13 CaPsol MLSA genotypes were detected in D. europaea (7) and plants (8). Nine of them corresponded to previously identified genotypes. Two new genotypes were found in D. europaea (tuf-b1/S1/V14/Rqg50-sv1 and tuf-b1/S18/V14/Rqg50-sv1) and one in Convolvulus arvensis (tuf-b1/S1/V2-TA/Rqg31-sv1), whereas one was shared by two hosts, Crepis foetida and Daucus carota (tuf-b1/S1/V2-TA/STOL-sv1). Naturally infected D. europaea successfully transmitted the tuf-b1/S1/V2-TA/STOL type to five grapevines and six periwinkles, tuf-b1/S1/V2-TA/Rqg31 to one grapevine, and tuf-b1/S1/V2-TA/Rqg50 to one periwinkle, indicating that D. europaea is an intermediate vector in CaPsol epidemiological cycles.

[1]  M. Kube,et al.  Multilocus Genotyping of ‘Candidatus Phytoplasma solani’ Associated with Rubbery Taproot Disease of Sugar Beet in the Pannonian Plain , 2021, Microorganisms.

[2]  M. Mitrović,et al.  Symptomatology, (Co)occurrence and Differential Diagnostic PCR Identification of ‘Ca. Phytoplasma solani’ and ‘Ca. Phytoplasma convolvuli’ in Field Bindweed , 2021, Pathogens.

[3]  A. Lucchi,et al.  Proposal of A New Bois Noir Epidemiological Pattern Related to ‘Candidatus Phytoplasma Solani’ Strains Characterized by A Possible Moderate Virulence in Tuscany , 2020, Pathogens.

[4]  P. Bianco,et al.  Identification and ecology of alternative insect vectors of ‘Candidatus Phytoplasma solani’ to grapevine , 2019, Scientific Reports.

[5]  M. Mitrović,et al.  Diversity of phytoplasmas identified in the polyphagous leafhopper Euscelis incisus (Cicadellidae, Deltocephalinae) in Serbia: pathogen inventory, epidemiological significance and vectoring potential , 2019, European Journal of Plant Pathology.

[6]  E. Verdin,et al.  Lavender Decline in France Is Associated with Chronic Infection by Lavender-Specific Strains of “Candidatus Phytoplasma solani” , 2018, Applied and Environmental Microbiology.

[7]  M. Mitrović,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 , 2018, European Journal of Plant Pathology.

[8]  M. Mitrović,et al.  Widespread plant specialization in the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), a major vector of stolbur phytoplasma: Evidence of cryptic speciation , 2018, PloS one.

[9]  P. Bodor,et al.  Bois noir affects the yield and wine quality of Vitis vinifera L. cv. ‘Chardonnay’ , 2018, European Journal of Plant Pathology.

[10]  E. Verdin,et al.  Important genetic diversity of ‘Candidatus Phytoplasma solani’ related strains associated with bois noir grapevine yellows and planthoppers in Azerbaijan , 2018, European Journal of Plant Pathology.

[11]  Haimin Chen,et al.  Molecular Identification and Diversity of ‘Candidatus Phytoplasma solani’ Associated with Red‐leaf Disease of Salvia miltiorrhiza in China , 2016 .

[12]  M. Radulović,et al.  Vmp1 and stamp genes variability of ‘Candidatus phytoplasma solani’ in Bosnian and Herzegovinian grapevine , 2016, European Journal of Plant Pathology.

[13]  M. Mitrović,et al.  ‘Candidatus phytoplasma solani’ genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (hemiptera, cixiidae) as natural vectors , 2016, European Journal of Plant Pathology.

[14]  M. Mitrović,et al.  Dictyophara europaea (Hemiptera: Fulgoromorpha: Dictyopharidae): description of immatures, biology and host plant associations , 2016, Bulletin of Entomological Research.

[15]  I. Toševski,et al.  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) , 2016 .

[16]  M. Maixner.  Transmission of German grapevine yellows (Vergilbungskrankheit) by the planthopper Hyalesthes obsoletus (Auchenorrhyncha: Cixiidae) , 2015 .

[17]  M. Maixner,et al.  Molecular characterisation of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA , 2015 .

[18]  J. Larrue,et al.  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 , 2015 .

[19]  M. Mitrović,et al.  The molecular epidemiology of bois noir grapevine yellows caused by ‘Candidatus Phytoplasma solani’ in the Republic of Macedonia , 2015, European Journal of Plant Pathology.

[20]  D. Škorić,et al.  A case study of FD and BN phytoplasma variability in Croatia: multigene sequence analysis approach , 2015, European Journal of Plant Pathology.

[21]  G. Brader,et al.  An abundant ‘Candidatus Phytoplasma solani’ tuf b strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus , 2014, European Journal of Plant Pathology.

[22]  M. Mitrović,et al.  Experimental and molecular evidence of Reptalus panzeri as a natural vector of bois noir , 2014 .

[23]  Wei Wei,et al.  'Candidatus Phytoplasma solani', a novel taxon associated with stolbur- and bois noir-related diseases of plants. , 2013, International journal of systematic and evolutionary microbiology.

[24]  M. Mitrović,et al.  First Report of Alder Yellows Phytoplasma Infecting Common and Grey Alder (Alnus glutinosa and A. incana) in Montenegro. , 2013, Plant disease.

[25]  X. Foissac,et al.  Impact of Vector Dispersal and Host-Plant Fidelity on the Dissemination of an Emerging Plant Pathogen , 2012, PloS one.

[26]  M. Mitrović,et al.  Characterisation of a 16SrII phytoplasma strain associated with bushy stunt of hawkweed oxtongue (Picris hieracioides) in south-eastern Serbia and the role of the leafhopper Neoaliturus fenestratus (Deltocephalinae) as a natural vector , 2012, European Journal of Plant Pathology.

[27]  X. Foissac,et al.  The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. , 2011, Gene.

[28]  X. Foissac,et al.  Genetic variability of the stolbur phytoplasma vmp1 gene in grapevines, bindweeds and vegetables , 2010, Journal of applied microbiology.

[29]  I. Toševski,et al.  Occurrence and Distribution of Grapevine Yellows Caused by Stolbur Phytoplasma in Montenegro , 2009 .

[30]  L. Filippin,et al.  Molecular characteristics of phytoplasmas associated with Flavescence dorée in clematis and grapevine and preliminary results on the role of Dictyophara europaea as a vector. , 2009 .

[31]  M. Mitrović,et al.  Stolbur phytoplasma transmission to maize by Reptalus panzeri and the disease cycle of maize redness in Serbia. , 2009, Phytopathology.

[32]  X. Foissac,et al.  GENETIC VARIABILITY OF STOLBUR PHYTOPLASMA IN ANNUAL CROP AND WILD PLANT SPECIES IN SOUTH MORAVIA , 2009 .

[33]  X. Foissac,et al.  Striking Diversity of vmp1, a Variable Gene Encoding a Putative Membrane Protein of the Stolbur Phytoplasma , 2009, Applied and Environmental Microbiology.

[34]  A. Liang,et al.  The Palaearctic Planthopper Genus Dictyophara Germar, 1833 (Hemiptera: Fulgoroidea: Dictyopharidae) in China , 2008 .

[35]  A. Seitz,et al.  Invasion biology and host specificity of the grapevine yellows disease vector Hyalesthes obsoletus in Europe , 2008 .

[36]  K. Izadpanah,et al.  Characterization of a Phytoplasma Associated with Cabbage Yellows in Iran. , 2007, Plant disease.

[37]  M. Mitrović,et al.  Roles of stolbur phytoplasma and Reptalus panzeri (Cixiinae, Auchenorrhyncha) in the epidemiology of Maize redness in Serbia , 2007, European Journal of Plant Pathology.

[38]  E. Verdin,et al.  "Candidatus Phlomobacter fragariae" Is the Prevalent Agent of Marginal Chlorosis of Strawberry in French Production Fields and Is Transmitted by the Planthopper Cixius wagneri (China). , 2003, Phytopathology.

[39]  X. Daire,et al.  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 , 1997, European Journal of Plant Pathology.

[40]  M. Mitrović,et al.  Wolbachia infection in natural populations of Dictyophara europaea, an alternative vector of grapevine Flavescence dorée phytoplasma: effects and interactions , 2018 .

[41]  D. Thiéry,et al.  Minor cultures as hosts for vectors of extensive crop diseases: Does Salvia sclarea act as a pathogen and vector reservoir for lavender decline? , 2017, Journal of Pest Science.

[42]  C. D.,et al.  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 , 2015 .

[43]  M. Mitrović,et al.  Potential new hemipteran vectors of stolbur phytoplasma in Serbian vineyards. , 2011 .

[44]  M. Mitrović,et al.  Molecular detection of potato stolbur phytoplasma in Serbia. , 2011 .

[45]  A. Omar,et al.  StAMP encoding the antigenic membrane protein of stolbur phytoplasma is useful for molecular epidemiology , 2011 .

[46]  P. Weintraub,et al.  Phytoplasma epidemiological systems with multiple plant hosts. , 2009 .

[47]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.