Transmission of Turnip yellows virus by Myzus persicae Is Reduced by Feeding Aphids on Double-Stranded RNA Targeting the Ephrin Receptor Protein

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.

Insect cuticular proteins and their role in transmission of phytoviruses

“…Cuticular proteins now feature prominently on the shortlist of insect molecules demonstrated to play a key role in plant virus transmission [ 12 •• , 13 •• , 14 •• , 15 •• ]. Recent literature has revealed that CuPs—the most obvious candidates as receptors for noncirculative viruses — also interact with plant circulative viruses.…”

“…These include structural proteins, membrane viral glycoproteins, or non-structural virus-encoded proteins [ 4 , 9 , 10 ]. However, an extensive study of virus–vector interactions at the molecular level is still challenged by the difficulty of identifying vector partners and validating their role in virus transmission [ 11 •• , 12 •• , 13 •• , 14 •• , 15 •• ].…”

Characterization of Papaya ringspot virus isolates infecting transgenic papaya ‘Huanong No.1’ in South China

“…Mulot et al . 34 revealed that the membrane-bound Ephrin receptor (Eph) in Myzus persicae is a novel aphid protein which is involved in the transmission of the Turnip yellows virus (TuYV) and further confirmed that the minor capsid protein of TuYV, essential for aphid transmission, was able to bind the external domain of Eph in yeast. Therefore, the addition or deletion of amino acids in the ‘EK’ region may influence aphids on the transmission of PRSV, so that the original dominant strain cannot be effectively and continuously transmitted.…”

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“…It has been recorded in Tunisia on pepper crops and several other crops and it causes big problems for pepper production (Ben-Halima Kamel, 2011). A moderate or high density of this aphid causes direct damage by sucking plant sap thereby inducing the deformation of plant leaves and indirect damage caused either by honeydew production or by transmission of plant viral diseases (Satar et al, 2008;Mulot et al, 2018). This can drastically restrain plant growth rates and result in reduced yield.…”