Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission
Open Access
- 1 March 2011
- journal article
- research article
- Published by American Society for Microbiology in Journal of Virology
- Vol. 85 (5), 2148-2166
- https://doi.org/10.1128/jvi.01504-10
Abstract
Yellow dwarf viruses in the family Luteoviridae, which are the causal agents of yellow dwarf disease in cereal crops, are each transmitted most efficiently by different species of aphids in a circulative manner that requires the virus to interact with a multitude of aphid proteins. Aphid proteins differentially expressed in F2 Schizaphis graminum genotypes segregating for the ability to transmit Cereal yellow dwarf virus-RPV (CYDV-RPV) were identified using two-dimensional difference gel electrophoresis (DIGE) coupled to either matrix-assisted laser desorption ionization-tandem mass spectrometry or online nanoscale liquid chromatography coupled to electrospray tandem mass spectrometry. A total of 50 protein spots, containing aphid proteins and proteins from the aphid9s obligate and maternally inherited bacterial endosymbiont, Buchnera, were identified as differentially expressed between transmission-competent and refractive aphids. Surprisingly, in virus transmission-competent F2 genotypes, the isoelectric points of the Buchnera proteins did not match those in the maternal Buchnera proteome as expected, but instead they aligned with the Buchnera proteome of the transmission-competent paternal parent. Among the aphid proteins identified, many were involved in energy metabolism, membrane trafficking, lipid signaling, and the cytoskeleton. At least eight aphid proteins were expressed as heritable, isoelectric point isoform pairs, one derived from each parental lineage. In the F2 genotypes, the expression of aphid protein isoforms derived from the competent parental lineage aligned with the virus transmission phenotype with high precision. Thus, these isoforms are candidate biomarkers for CYDV-RPV transmission in S. graminum. Our combined genetic and DIGE approach also made it possible to predict where several of the proteins may be expressed in refractive aphids with different barriers to transmission. Twelve proteins were predicted to act in the hindgut of the aphid, while six proteins were predicted to be associated with the accessory salivary glands or hemolymph. Knowledge of the proteins that regulate virus transmission and their predicted locations will aid in understanding the biochemical mechanisms regulating circulative virus transmission in aphids, as well as in identifying new targets to block transmission.This publication has 84 references indexed in Scilit:
- The Transmission Efficiency of Tomato Yellow Leaf Curl Virus by the Whitefly Bemisia tabaci Is Correlated with the Presence of a Specific Symbiotic Bacterium SpeciesJournal of Virology, 2010
- The “acrostyle”: A newly described anatomical structure in aphid styletsArthropod Structure & Development, 2010
- Identification of Quantitative Trait Loci Underlying Proteome Variation in Human Lymphoblastoid CellsMolecular & Cellular Proteomics, 2010
- Genetic Heterogeneity in Human DiseaseCell, 2010
- Measurement of Human Surfactant Protein-B Turnover in Vivo from Tracheal Aspirates Using Targeted ProteomicsAnalytical Chemistry, 2010
- Annotation and analysis of low‐complexity protein families of Anopheles gambiae that are associated with cuticleInsect Molecular Biology, 2009
- CDD: specific functional annotation with the Conserved Domain DatabaseNucleic Acids Research, 2009
- Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networksProceedings of the National Academy of Sciences of the United States of America, 2007
- Gapped BLAST and PSI-BLAST: a new generation of protein database search programsNucleic Acids Research, 1997
- Binding of nidogen and the laminin‐nidogen complex to basement membrane collagen type IVEuropean Journal of Biochemistry, 1989