# Recent advances in grapevine phytoplasma research

Xavier Foissac

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Xavier Foissac. Recent advances in grapevine phytoplasma research. 20th Conference of the International Council for the Study of Virus and Virus-Like Diseases of the Grapevine, University of Thessaloniki, Sep 2023, Thessaloniki, Greece. hal-04700122

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# Recent advances in grapevine phytoplasma research

Xavier, Foissac¹*

¹Univ. Bordeaux, INRAE, UMR BFP, Villenave d'Ornon 33882 CEDEX, France.

*Corresponding author(s): xavier.foissac@inrae.fr

## INTRODUCTION

Grapevine yellows are phytoplasma-associated diseases mainly characterized by leaf discoloration, shriveling of grapes and non-lignification of infected canes. These diseases have been reported in all grapevine growing areas and are associated with different phytoplasmas depending on the continent. The epidemiology of phytoplasmoses is dictated by the biology and ecology of the insect vector. If the vector carries out its life cycle on the infected crop, the outbreaks are characterized by the aggregation of diseased plants which are all the more abundant as the vector population is high. This is particularly the case for the grapevine Flavescence dorée (FD), which is transmitted in Europe by the ampelophagous leafhopper *Scaphoideus titanus*. Since the sequencing of phytoplasma genomes in the 2000s, genomics data provided genetic markers that have greatly facilitated the understanding of phytoplasma epidemiological cycles unveiling for instance the unexpected complexity of Bois noir phytoplasma ecology. The discovery of phytoplasma surface proteins implicated in the adaptation of phytoplasmas to different insect vectors allowed to distinguish epidemic and non-epidemic strains of FD phytoplasmas. The development of phenotyping protocols and comparative field trials is opening new perspectives in the identification of grapevine genetic determinants governing contrasted susceptibility of grapevine cultivars to FD.

## NEW EPIDEMIOLOGICAL CYCLES INVESTIGATED

Multilocus sequencing strategies have facilitated to deciphering of different propagation pathways involving different plant reservoirs and insect vectors. Two “*Ca*. P. solani” genetic markers encoding surface proteins submitted to strong positive selections serve has powerful markers for the molecular epidemiology of “*Candidatus* Phytoplasma solani”, the agent of grapevine Bois noir. For instance, new epidemiological cycles have recently been discovered that involves the planthopper *Hyalesthes obsoletus* propagating the phytoplasma from *Crepis faetida* (Kosovac et al., 2019). In addition to *Hyalesthes obsoletus* and *Reptalus panzeri*, *Dictyophara europaea* was also shown to experimentally transmit “*Ca*. P. solani” to grapevine (Curkovic et al., 2022). The use of genetic markers associated to large scale ecological surveys and vector transmission also allowed to decipher the origin of FD. Since the first outbreaks in Southwestern France, FD epidemics had been associated to the introduction of the North American leafhopper vector *Scaphoideus titanus*. It was recently demonstrated that FD phytoplasma originated from European alders and that epidemics in grapevine are restricted to some genetic variants pre-existing in alders. The compatibility of these variants to the introduced *S. titanus* insect vector resulted from the adaptation of phytoplasma variable membrane proteins Vmps to leafhoppers of the same subfamily living on alders. Therefore, alternative vectors and new reservoir plants have been identified (Malembic-Maher et al., 2020).

## INTERACTION WITH INSECT VECTORS

The process of insect cells colonization requires adhesion and internalization steps. It was shown that the membrane protein VmpA of the FD phytoplasma acts as an adhesin able to interact with cells of its leafhopper vector *Euscelidius variegatus* and *S. titanus* (Arricau-Bouvery et al., 2018). VmpA binds insect glycoproteins via a lectin activity (Arricau-Bouvery et al., 2021) and the FD phytoplasma enters
insect vector cells via a clathrin-mediated endocytosis (Arricau-Bouvery et al., 2023). Phytoplasma surface proteins like AMP or the IMP interacts with the insect vector actin microfilaments, a phenomenon certainly involved in the intracellular trafficking of phytoplasmas.

## GENETIC BASIS OF GRAPEVINE SUSCEPTIBILITY TO PHYTOPLASMA

Upon surveys cultivar Cabernet Sauvignon was found highly susceptible to FD, with high proportion of symptomatic branches and high phytoplasma titers, in contrast to Merlot. Localized insect transmissions and grafting showed that phytoplasma circulate in the whole plant in Cabernet Sauvignon, while in Merlot they are restricted to the transmission point. Phenotyping using insect-mediated transmission allowed to classify 28 Vitis accessions into three distinct categories, according to the percentage of infected plants and their phytoplasma titers. Reduced symptoms in the *Vitis vinifera* cultivars was associated to low phytoplasma titers and low percentages of infected plants. The low susceptibility of Merlot was observed for one of its parents, i.e., Magdeleine Noire des Charentes (Eveillard et al., 2016). The same confinement of symptoms and FD phytoplasma was observed in cultivar Tocai Friulani and correlated with high activation of both jasmonate- and salicylate-mediated responses, together with a great accumulation of resveratrol (Casarin et al., 2023). In conclusion, cultivars carrying traits of reduced susceptibility to FD have been identified and might be used as future genitors and provide genetic markers to select cultivars with reduced susceptibility to FD.

## ACKNOWLEDGEMENTS

This communication was supported by the Plan National Dépérissement du Vignoble grant Co-Act2.

## REFERENCES

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Arricau-Bouvery, N., Duret, S., Dubrana, M-P., Desqué, D., Eveillard, S., Brocard, L., Malembic-Maher, S., Foissac, X. 2021. Interactions between the flavescence dorée phytoplasma and its insect vector indicate lectin-type adhesion mediated by the adhesin VmpA. Scientific Reports. 11:11222 https://doi.org/10.1038/s41598-021-90809-z

Arricau-Bouvery, N., Dubrana, M-P., Canuto F., Duret, S., Brocard, L., Claverol, S., Malembic-Maher, S., Foissac, X. 2023. Flavescence dorée phytoplasma enters insect cells by a clathrin-mediated endocytosis allowing infection of its insect vector. Scientific Reports. 13:2211 https://doi.org/10.1038/s41598-023-29341-1

Casarin, S., Vincenzi, S., Esposito, A., Filippin, L., Forte, V., Angelini, E., Bertazzon, N. 2023. A successful defence strategy in grapevine cultivar 'Tocai friulano' provides compartimentation of grapevine Flavescence dorée phytoplasma. BMC Plant Biology. 23:161. https://doi.org/10.1186/s12870-023-04122-0

Cvrković, T., Jović, J., Krstić, O., Marinković, S., Jakovljević, M., Mitrović, M., Toševski, I. 2022. Epidemiological Role of *Dictyophara europaea* (Hemiptera: Dictyopharidae) in the Transmission of 'Candidatus Phytoplasma solani'. Horticulturae. 8, 654. https://doi.org/10.3390/horticulturae8070654

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Kosovac, A., Jakovljević, M., Krstić, O., Cvrković, T., Mitrović, M., Toševski, I., Jović, J. 2019. 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. European Journal of Plant Pathology. 153:183-195. https://doi.org/10.1007/s10658-018-1553-1

Malembic-Maher, S., Desqué, D., Khalil, D., Salar, P., Bergey, B., Danet, J.-L., et al. 2020. When a palearctic bacterium meets a neararctic insect vector: genetic and ecological insights into the emergence of the grapevine flavescence dorée epidemics in Europe. PloS Pathog. 16 (3) e1007967. https://doi.org/10.1371/journal.ppat.1007967