Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects.

Elena Gonella,Elena Crotti,Massimo Marzorati,Alberto Alma,Bessem Chouaia,Mauro Mandrioli,Massimo Pajoro,Ilaria Negri,Daniela Bulgari,Daniele Daffonchio,Marianna Pontini,Luciano Sacchi

doi:10.1038/srep15811

Abstract

Intracellular reproductive manipulators, such as Candidatus Cardinium and Wolbachia are vertically transmitted to progeny but rarely show co-speciation with the host. In sap-feeding insects, plant tissues have been proposed as alternative horizontal routes of interspecific transmission, but experimental evidence is limited. Here we report results from experiments that show that Cardinium is horizontally transmitted between different phloem sap-feeding insect species through plants. Quantitative PCR and in situ hybridization experiments indicated that the leafhopper Scaphoideus titanus releases Cardinium from its salivary glands during feeding on both artificial media and grapevine leaves. Successional time-course feeding experiments with S. titanus initially fed sugar solutions or small areas of grapevine leaves followed by feeding by the phytoplasma vector Macrosteles quadripunctulatus or the grapevine feeder Empoasca vitis revealed that the symbionts were transmitted to both species. Explaining interspecific horizontal transmission through plants improves our understanding of how symbionts spread, their lifestyle and the symbiont-host intermixed evolutionary pattern.

Highlights

Symbiont Coriobacterium glomerans of the red firebug Pyrrhocoris apterus and the symbionts of the firebrat Thermobia domestica are acquired horizontally by juveniles through symbiont-containing eggshells, faeces, or adult bugs[21,22]
By using the cicadellid Scaphoideus titanus, a Cardinium-holder strictly feeding on grapevine leaves, as a model, we show that Cardinium is released from the insect’s salivary glands to the plant tissues and horizontally acquired by other grapevine feeder and non-grapevine feeder insects
The first set of experiments was conducted to assess the capability of S. titanus to release Cardinium during feeding on an artificial substrate or on grapevine leaves

Summary

Introduction

Symbiont Coriobacterium glomerans of the red firebug Pyrrhocoris apterus and the symbionts of the firebrat Thermobia domestica are acquired horizontally by juveniles through symbiont-containing eggshells, faeces, or adult bugs[21,22]. Direct demonstrations of intra- or inter-specific horizontal transmission of Wolbachia from the host to a parasitoid[29], or in parasitoids sharing the same host eggs[30,31], have been reported in few host models. We demonstrate that an inter-specific horizontal transmission of Cardinium can take place in leafhoppers and that such a transmission occurs through the plant tissue pierced by the insect host. By using the cicadellid Scaphoideus titanus, a Cardinium-holder strictly feeding on grapevine leaves, as a model, we show that Cardinium is released from the insect’s salivary glands to the plant tissues and horizontally acquired by other grapevine feeder and non-grapevine feeder insects

Methods

Results

Conclusion