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Abstract
Aphid-transmitted plant viruses are a threat for major crops causing massive economic loss worldwide. Members in the Luteoviridae family are transmitted by aphids in a circulative and non-replicative mode. Virions are acquired by aphids when ingesting sap from infected plants and are transported through the gut and the accessory salivary gland (ASG) cells by a transcytosis mechanism relying on virus-specific receptors largely unknown. Once released into the salivary canal, virions are inoculated to plants, together with saliva, during a subsequent feeding. In this paper, we bring in vivo evidence that the membrane-bound Ephrin receptor (Eph) is a novel aphid protein involved in the transmission of the Turnip yellows virus (TuYV, Polerovirus genus, Luteoviridae family) by Myzus persicae. The minor capsid protein of TuYV, essential for aphid transmission, was able to bind the external domain of Eph in yeast. Feeding M. persicae on in planta- or in vitro-synthesized dsRNA targeting Eph-mRNA (dsRNAEph) did not affect aphid feeding behavior but reduced accumulation of TuYV genomes in the aphid's body. Consequently, TuYV transmission efficiency by the dsRNAEph-treated aphids was reproducibly inhibited and we brought evidence that Eph is likely involved in intestinal uptake of the virion. The inhibition of virus uptake after dsRNAEph acquisition was also observed for two other poleroviruses transmitted by M. persicae, suggesting a broader role of Eph in polerovirus transmission. Finally, dsRNAEph acquisition by aphids did not affect nymph production. These results pave the way toward an ecologically safe alternative of insecticide treatments that are used to lower aphid populations and reduce polerovirus damages.
Highlights
To circumvent plant immobility, and escape before the plant dies, the majority of plant viruses rely on mobile vectors for their dissemination
Other aphid proteins exhibiting the ability to bind purified luteovirids in vitro have been reported but their precise role in virus transmission has not been identified. This includes several proteins extracted from Myzus persicae or heads of Sitobion avenae which exhibited the capacity to bind to virions of Turnip yellows virus (TuYV), previously designated Beet western yellows virus (Seddas et al, 2004), or of Barley yellow dwarf virus (BYDV) (Li et al, 2001)
In order to identify partners of polerovirus particles in the aphid M. persicae, we looked for cellular partners of the structural proteins of Cucurbit aphid borne yellows virus (CABYV) which is efficiently transmitted by this aphid species (Lecoq et al, 1992)
Summary
Escape before the plant dies, the majority of plant viruses rely on mobile vectors for their dissemination. The gut membrane protein alanyl aminopeptidase N (APN), was identified previously as a potential receptor of pea enation mosaic virus (PEMV, Enamovirus genus, Luteoviridae family) in the aphid species A. pisum using an array of in vitro-based techniques and insect cells experiments (Linz et al, 2015). Other aphid proteins exhibiting the ability to bind purified luteovirids in vitro have been reported but their precise role in virus transmission has not been identified This includes several proteins extracted from Myzus persicae or heads of Sitobion avenae which exhibited the capacity to bind to virions of Turnip yellows virus (TuYV), previously designated Beet western yellows virus (Seddas et al, 2004), or of Barley yellow dwarf virus (BYDV) (Li et al, 2001). These results implicate Eph in the transmission process of TuYV and suggest involvement of this protein in transmission of other poleroviruses by M. persicae
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