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Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of cereal yellow dwarf virus.

ABSTRACT: Yellow dwarf viruses cause the most economically important virus diseases of cereal crops worldwide and are transmitted by aphid vectors. The identification of aphid genes and proteins mediating virus transmission is critical to develop agriculturally sustainable virus management practices and to understand viral strategies for circulative movement in all insect vectors. Two cyclophilin B proteins, S28 and S29, were identified previously in populations of Schizaphisgraminum that differed in their ability to transmit the RPV strain of Cereal yellow dwarf virus (CYDV-RPV). The presence of S29 was correlated with F2 genotypes that were efficient virus transmitters. The present study revealed the two proteins were isoforms, and a single amino acid change distinguished S28 and S29. The distribution of the two alleles was determined in 12 F2 genotypes segregating for CYDV-RPV transmission capacity and in 11 genetically independent, field-collected S. graminum biotypes. Transmission efficiency for CYDV-RPV was determined in all genotypes and biotypes. The S29 isoform was present in all genotypes or biotypes that efficiently transmit CYDV-RPV and more specifically in genotypes that efficiently transport virus across the hindgut. We confirmed a direct interaction between CYDV-RPV and both S28 and S29 using purified virus and bacterially expressed, his-tagged S28 and S29 proteins. Importantly, S29 failed to interact with a closely related virus that is transported across the aphid midgut. We tested for in vivo interactions using an aphid-virus co-immunoprecipitation strategy coupled with a bottom-up LC-MS/MS analysis using a Q Exactive mass spectrometer. This analysis enabled us to identify a third cyclophilin protein, cyclophilin A, interacting directly or in complex with purified CYDV-RPV. Taken together, these data provide evidence that both cyclophilin A and B interact with CYDV-RPV, and these interactions may be important but not sufficient to mediate virus transport from the hindgut lumen into the hemocoel.

SUBMITTER: Tamborindeguy C

PROVIDER: S-EPMC3739738 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of cereal yellow dwarf virus.

Tamborindeguy Cecilia C Bereman Michael S MS DeBlasio Stacy S Igwe David D Smith Dawn M DM White Frank F MacCoss Michael J MJ Gray Stewart M SM Cilia Michelle M

PloS one 20130809 8

Yellow dwarf viruses cause the most economically important virus diseases of cereal crops worldwide and are transmitted by aphid vectors. The identification of aphid genes and proteins mediating virus transmission is critical to develop agriculturally sustainable virus management practices and to understand viral strategies for circulative movement in all insect vectors. Two cyclophilin B proteins, S28 and S29, were identified previously in populations of Schizaphisgraminum that differed in thei ...[more]

PMID: 23951206

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Project description:BACKGROUND:Schizaphis graminum is one of the most important and devastating cereal aphids worldwide, and its feeding can cause chlorosis and necrosis in wheat. However, little information is available on the wheat defence responses triggered by S. graminum feeding at the molecular level. RESULTS:Here, we collected and analysed transcriptome sequencing data from leaf tissues of wheat infested with S. graminum at 2, 6, 12, 24 and 48?hpi (hours post infestation). A total of 44,835 genes were either up- or downregulated and differed significantly in response to aphid feeding. The expression levels of a number of genes (9761 genes) were significantly altered within 2 hpi and continued to change during the entire 48?h experiment. Gene Ontology analysis showed that the downregulated DEGs were mainly enriched in photosynthesis and light harvesting, and the total chlorophyll content in wheat leaves was also significantly reduced after S. graminum infestation at 24 and 48?hpi. However, a number of related genes of the salicylic acid (SA)-mediated defence signalling pathway and MAPK-WRKY pathway were significantly upregulated at early feeding time points (2 and 6 hpi). In addition, the gene expression and activity of antioxidant enzymes, such as peroxidase and superoxide dismutase, were rapidly increased at 2, 6 and 12 hpi. DAB staining results showed that S. graminum feeding induced hydrogen peroxide (H2O2) accumulation at the feeding sites at 2 hpi, and increased H2O2 production was detected with the increases in aphid feeding time. Pretreatment with diphenylene iodonium, an NADPH oxidase inhibitor, repressed the H2O2 accumulation and expression levels of SA-associated defence genes in wheat. CONCLUSIONS:Our transcriptomic analysis revealed that defence-related pathways and oxidative stress in wheat were rapidly induced within hours after the initiation of aphid feeding. Additionally, NADPH oxidase plays an important role in aphid-induced defence responses and H2O2 accumulation in wheat. These results provide valuable insight into the dynamic transcriptomic responses of wheat leaves to phytotoxic aphid feeding and the molecular mechanisms of aphid-plant interactions.

Dataset Information

Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of cereal yellow dwarf virus.

Publications

Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of cereal yellow dwarf virus.

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