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Vector Transmission of a Plant-Pathogenic Bacterium in the Arsenophonus Clade Sharing Ecological Traits with Facultative Insect Endosymbionts

First, second, third, and fifth authors: Biologie et écologie des bactéries du phloème, UMR Plante Microbe Environnement INRA--CNRS--Université de Bourgogne, BP 86510--21065 DIJON Cedex France; and fourth author: Centre de microscopie électronique, UMR Plante Microbe Environnement INRA--CNRS--Université de Bourgogne, BP 86510--21065 DIJON Cedex.

The planthopper Pentastiridius leporinus (Hemiptera: Cixiidae) is the major vector of a nonculturable plant-pathogenic γ-3 proteobacterium associated with a disease of sugar beet called syndrome “basses richesses” (SBR). The bacterium, here called SBR bacterium, belongs to the Arsenophonous clade, which includes mostly insect-associated facultative symbionts. Assays using field-collected planthopper nymphs and adults were carried out to investigate the interaction of SBR bacterium with the insect vector and its transmission to sugar beet. Field-collected planthoppers showed a percentage of infection that averaged from 57% for early instar nymphs to near 100% for late instar nymphs and emerging adults. SBR bacterium was persistently transmitted by emerging adults. Root-feeding nymphs were able to inoculate SBR bacterium to sugar beet. The bacterium was transmitted vertically from infected parental females to their respective offspring with an average frequency of 30%. Real-time polymerase chain reaction assays on dissected planthopper internal organs revealed a high concentration of the bacterium within male and female reproductive organs and within female salivary glands. SBR-like bacteria were observed through transmission electron microscopy in the cytoplasm of different insect organs including ovaries, salivary glands, and guts with no evidence for cytological disorders. SBR bacterium seems to share common ecological traits of insect-transmitted plant pathogens and facultative insect endosymbionts suggesting it may have evolved primarily as an insect-associated bacterium.

Additional keywords:“Candidatus Phlomobacter fragariae”, Cixius wagneri, phloem-limited bacteria.