Multi-scale spatial genetic structure of the vector-borne pathogen \u2018Candidatus Phytoplasma prunorum\u2019 in orchards and in wild habitats

Véronique Marie-Jeanne,Nicolas Sauvion,François Bonnot,Gaël Thébaud,Jean Peccoud,Gérard Labonne

doi:10.1038/s41598-020-61908-0

Abstract

Inferring the dispersal processes of vector-borne plant pathogens is a great challenge because the plausible epidemiological scenarios often involve complex spread patterns at multiple scales. The spatial genetic structure of ‘Candidatus Phytoplasma prunorum’, responsible for European stone fruit yellows disease, was investigated by the application of a combination of statistical approaches to genotype data of the pathogen sampled from cultivated and wild compartments in three French Prunus-growing regions. This work revealed that the prevalence of the different genotypes is highly uneven both between regions and compartments. In addition, we identified a significant clustering of similar genotypes within a radius of 50 km or less, but not between nearby wild and cultivated Prunus. We also provide evidence that infected plants are transferred between production areas, and that both species of the Cacopsylla pruni complex can spread the pathogen. Altogether, this work supports a main epidemiological scenario where ‘Ca. P. prunorum’ is endemic in — and generally acquired from — wild Prunus by its immature psyllid vectors. The latter then migrate to shelter plants that epidemiologically connect sites less than 50 km apart by later providing infectious mature psyllids to their “migration basins”. Such multi-scale studies could be useful for other pathosystems.

Highlights

Inferring the dispersal processes of vector-borne plant pathogens is a great challenge because the plausible epidemiological scenarios often involve complex spread patterns at multiple scales
Deciphering the complexity of plausible epidemiological scenarios poses a great challenge, especially since insects are involved in disease spread
The spatial scale of the processes has been a central question for decades in ecology[11,12,13,14] and population genetics[15,16], the development of large-scale pattern-oriented approaches to understand the processes that shape the genetic structure of a population is recent[17,18,19,20,21]

Summary

Introduction

Inferring the dispersal processes of vector-borne plant pathogens is a great challenge because the plausible epidemiological scenarios often involve complex spread patterns at multiple scales. The spatial genetic structure of ‘Candidatus Phytoplasma prunorum’, responsible for European stone fruit yellows disease, was investigated by the application of a combination of statistical approaches to genotype data of the pathogen sampled from cultivated and wild compartments in three French Prunus-growing regions. This work supports a main epidemiological scenario where ‘Ca. P. prunorum’ is endemic in — and generally acquired from — wild Prunus by its immature psyllid vectors The latter migrate to shelter plants that epidemiologically connect sites less than 50 km apart by later providing infectious mature psyllids to their “migration basins”. The spatial scale of these processes is unknown and, in combination with the landscape structure, this may lead to more or less complex epidemiological networks that connect close or distant ecological compartments (Supplementary Fig. S1)

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