ARS | Publication request: Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission

Submitted to: PLoS One
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 21, 2012
Publication Date: October 30, 2012
Citation: Cilia, M., Peter, K.A., Bereman, M., Howe, K.J., Fish, T., Smith, D., Gildow, F., Maccoss, M., Gray, S.M. 2012. Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission. PLoS One. 7(10).

Interpretive Summary: Many plant viruses are transmitted by sap sucking insects such as aphids and there are few effective options for preventing the spread of disease. Aphids acquire viruses when feeding on an infected plant and then carry the virus with them when they move to feed on another plant. The transmission process is very specific and only one or a few insect species can transmit each virus. We have discovered many of the aphid and virus proteins that interact with each other and regulate the transmission process, but here we report that plant proteins are also involved in how well a virus can be transmitted by an aphid. Serendipitously, we discovered that we could chemically change a virus so that it was no longer transmitted. Further investigation revealed that the changes in the virus did not directly cause the loss of transmission, but rather that was due to an alteration of plant proteins adhering to the virus. Using mass spectrometry methods several plant proteins were identified that bind to transmissible virus. Altering the surface features of the virus changes the suite of plant proteins associated with the virus and prevents the virus from moving through the various aphid tissues; a requirement for successful transmission. Knowing the details of the plant – virus protein interactions could allow for the development of novel strategies to disrupt the normal interactions and reduce the spread of disease.

Technical Abstract: The transmission of viruses in the Luteoviridae, such as Cereal yellow dwarf virus (CYDV), requires a series of precisely orchestrated interactions between virus proteins, plant proteins, and aphid proteins. These viruses are retained in the phloem for aphid acquisition and are transmitted by aphids in a circulative manner. We show that treatment of infected oat tissue homogenate with sodium sulfite reduces transmission of the purified virus by aphids. Transmission electron microscopy shows no gross change in virion morphology due to treatments. However, treated virions are not internalized into aphid hindgut epithelial cells and are not transmitted when injected directly into the hemocoel. LC-MS/MS analysis of virus preparations reveals a number of host plant proteins co-purifying with viruses, a number of which are lost following sodium sulfite treatment. Using targeted mass spectrometry, we show that several of the virus-associated host plant proteins accumulate to higher levels in aphids that have fed on CYDV infected plants as compared to healthy plants. We propose that sodium sulfite treatment disrupts critical virion-host protein interactions required for aphid transmission and that disulfide bonding is essential for protein-protein interactions during virus entry into aphid cells.