Identification of the first plant virus receptors in aphids

Plant health: how to stop virus transmission by aphids

A few months apart, two scientists from Inra publish their work on the characterization of the mechanisms underlying virus transmission by aphids. These studies should pave the way for novel control methods of viral spread.

Plant viruses are widespread in many crops around the world, and cause important yield and economic loss. They are propagated by mobile plant-feeding organisms called vectors that transport the virus from plant to plant. Aphids are the most frequent and economically important vectors of plant viruses, transmitting hundreds of viral species. Current control methods mainly rely on chemicals, known for their negative impact on the environment and on human health.

Among other ongoing alternatives studied at Inra (resistant crops, biocontrol, …), deciphering the molecular mechanisms underlying virus transmission by aphids seems a promising prospect. The identification of virus receptors in insects and the understanding of their function in virus transmission should help developing strategies to specifically target and disrupt virus/vector interactions and thus impair viral spread in crops.

Two researchers from the Plant Health and Environment Division of Inra, Marilyne Uzest (UMR BGPI¹, group of Stéphane Blanc) and Véronique Brault (UMR SVQV²), have worked on two distinct virus models, noncirculative viruses located on aphid mouthparts, and circulative viruses transported through the insect’s body. Today, they publish their results and shed light on a topic still poorly documented and yet a very promising developing field for alternatives to chemicals.

Marilyne Uzest main focus is on noncirculative viruses retained on the stylets, the aphid mouthparts, while Véronique Brault is working on circulative viruses that pass through gut and salivary glands cells.

Proteins involved in plant virus transmission by aphids

They identified two proteins involved in virus transmission by aphids using an RNA-interfering based technology referred to as “gene silencing”. This technology allows the knockdown of gene expression, and hence reduces the amount of the corresponding protein in aphids. Marilyne Uzest and her colleagues showed that decreasing the expression of “stylin-1” identified in aphid stylets impacted Cauliflower mosaic virus transmission by the insect. In the case of the “Ephrin receptor” protein, the group of Véronique Brault observed a significant reduction in the transmission of Turnip yellows virus by aphids. It is the first report of virus transmission inhibition by targeting specific aphid proteins.

In the BGPI unit of Montpellier, Marilyne Uzest has previously set up an original approach to immunolabel dissected stylets. Together with high-resolution microscopy observations, she discovered a tiny organ in aphid stylets, which was named acrostyle. The production of a library of antibodies (70) specifically targeting aphid cuticular proteins conducted to the identification of the first proteins ever characterized in insect mouthparts, among which Stylin 1 located in the acrostyle.

In the SVQV unit in Colmar, the group of Véronique Brault looked for aphid proteins able to bind to virus particles. Interactions between the viral coat proteins and the aphid proteins were obtained and among the candidates they identified the Ephrin receptor protein.

Towards novel control strategies to limit of viral spread

These data provided unprecedented insights into the molecular mechanisms involved in virus transmission by aphids. The work contributed to the development of novel tools and innovative approaches to study the virus transmission mechanisms in aphid vectors. Now, the two groups are pursuing their efforts on the characterization of aphid receptors for agriculturally important viruses. They would like to know whether stylin-1 is a generic receptor broadly used by noncirculative viruses, and whether Ephrin receptor is involved in the transmission of other circulative viruses such as those infecting potato or sugar beet crops.

Efforts to identify virus receptors and their potential co-factors must be pursued. A comprehensive characterization of these molecules would help targeting virus retention in aphids. These studies should lead to innovative control methods of viral spread by disrupting virus transmission by aphids.

¹ BGPI Biology and genetics of plant-pathogen interactions
² SVQV Grapevine health and wine quality

Projects

2007-2011. ANR project Virus-Vection - Partners Inra http://www.agence-nationale-recherche.fr/Projet-ANR-07-BLAN-0203 

2012-2014. Grand Challenge Explorations, phase I. Bill and Melinda Gates Foundation 

2012-2015. Grant « Chercheuse d’avenir » from Région Languedoc-Roussillon. Marilyne Uzest.

2013-2015. Post-doc grants from Inra-Plant Health and Environment Division

2015-2017. PhD grant from Région Grand-Est/Inra- Plant Health and Environment Division 2015-2018. Grand Challenge Explorations, phase II. F Bill and Melinda Gates FoundationPartners CNRS, Inserm, University of Lyon 1, CSIC - Madrid

2015-2019. ANR project StylHook - Partenaires Inra, CNRS, Inserm http://www.agence-nationale-recherche.fr/Projet-ANR-15-CE20-0011

References

• Transmission of Turnip yellows virus by Myzus persicae Is Reduced by Feeding Aphids on Double-Stranded RNA Targeting the Ephrin Receptor Protein - doi: 10.3389/fmicb.2018.00457
• Identification of plant virus receptor candidates in the stylets of their aphid vectors -  J. Virol. July 2018 92:e00432-18