Biometrical genetic analysis of luteovirus transmission in the aphid Schizaphis graminum

Burrows, Mary; Caillaud, Marina C.; Smith, Dawn; Gray, Stewart M.

doi:10.1038/sj.hdy.6800909

Cited by 31 publications

(30 citation statements)

References 66 publications

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“…The DIGE expression data were first compared between the three transmission-competent genotypes (Sg-F, A3, and CC6) and the refractive parent genotype Sg-SC. These spots were selected without regard to their expression in the refractive F2 genotypes, since the genes controlling virus transmission are additive in effect (8,9,34), and as we expected, the refractive F2 genotypes expressed some of the proteins in a manner similar to that of the competent genotypes. Thirty-two such spots were identified (Tables 2 and 3), 13 of which were aphid proteins upregulated in the competent genotypes and 7 of which were downregulated in the competent genotypes ( Table 2).…”

Section: Resultsmentioning

confidence: 99%

“…Parthenogenetically reproducing aphid colonies were maintained on caged barley (Hordeum vulgare) at 20°C with an 18-h photo period as described previously (35). The origins and CYDV-RPV transmission efficiencies of the parental genotypes of S. graminum, Sg-SC and Sg-F, as well as the F2 genotypes A3, C2, K2, and K3 were described previously (8,9,32,77). Additional F2 genotypes, MM1, BB1, CC1, and CC6, are described in Table 1.…”

Section: Methodsmentioning

confidence: 99%

“…The virus movement across potential transmission barriers also segregates independently in the F2 genotypes, indicating that the movement of virions across the gut and ASG is also controlled by different genes (8). Furthermore, genetic analyses of the F2 population indicated that virus transmission in this population is controlled by a few major genes and a multitude of minor genes acting in an additive manner (9,32).…”

mentioning

confidence: 96%

“…An F2 population segregating for yellow dwarf virus (YDV) transmission efficiency has been maintained as parthenogenetically reproducing genotypes, which allows repeated phenotyping of heritable traits. Genetic analysis of the F2 genotypes showed that the transmission of each YDV species is controlled by distinct but overlapping sets of loci (8,9,34). The virus movement across potential transmission barriers also segregates independently in the F2 genotypes, indicating that the movement of virions across the gut and ASG is also controlled by different genes (8).…”

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confidence: 99%

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Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission

Cilia

Tamborindeguy

Fish

et al. 2011

J Virol

103

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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 aphid's 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.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 96%

mentioning

confidence: 99%

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Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission

Cilia

Tamborindeguy

Fish

et al. 2011

J Virol

103

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“…Sexual crosses with aphids with these genotypes coupled with transmission efficiency studies on F 1 and F 2 progeny indicated that the hybrids segregated not only for the ability to transmit each virus species but also for which cellular barrier (hindgut or ASG) blocked virus movement and transmission (3). Subsequent genetic analysis indicated that genetic inheritance of vector competence was a multigenic trait involving only a few major genes and several minor genes that function in an additive manner (4). Evidence that multigenetic factors in aphids regulated luteovirus transmission is consistent with other work describing transmission barriers to luteovirus transmission occurring at different sites in aphid tissues, such as the gut and salivary gland (12).…”

mentioning

confidence: 99%

Coupling Genetics and Proteomics To Identify Aphid Proteins Associated with Vector-Specific Transmission of Polerovirus ( Luteoviridae )

Yang

Thannhauser²,

Burrows

et al. 2008

J Virol

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Cereal yellow dwarf virus-RPV (CYDV-RPV) is transmitted specifically by the aphids Rhopalosiphum padi andSchizaphis graminum in a circulative nonpropagative manner. The high level of vector specificity results from the vector aphids having the functional components of the receptor-mediated endocytotic pathways to allow virus to transverse the gut and salivary tissues. Studies of F 2 progeny from crosses of vector and nonvector genotypes of S. graminum showed that virus transmission efficiency is a heritable trait regulated by multiple genes acting in an additive fashion and that gut-and salivary gland-associated factors are not genetically linked. Utilizing two-dimensional difference gel electrophoresis to compare the proteomes of vector and nonvector parental and F 2 genotypes, four aphid proteins (S4, S8, S29, and S405) were specifically associated with the ability of S. graminum to transmit CYDV-RPV. The four proteins were coimmunoprecipitated with purified RPV, indicating that the aphid proteins are capable of binding to virus. Analysis by mass spectrometry identified S4 as a luciferase and S29 as a cyclophilin, both of which have been implicated in macromolecular transport. Proteins S8 and S405 were not identified from available databases. Study of this unique genetic system coupled with proteomic analysis indicated that these four virus-binding aphid proteins were specifically inherited and conserved in different generations of vector genotypes and suggests that they play a major role in regulating polerovirus transmission.Viruses in the family Luteoviridae, including Barley yellow dwarf virus (BYDV), Cereal yellow dwarf virus (CYDV), Potato leafroll virus, and Beet western yellows virus, are collectively referred to in this paper as luteovirids. They are transmitted in a circulative persistent nonpropagative manner only by aphids (Aphididae: Hemiptera) (20). Ultrastructural studies indicate that all luteovirids follow a similar pathway through their aphid vectors (12). Aphids acquire the viruses from infected phloem cells while feeding with their piercing-sucking stylets. Virions are drawn up the food canal of the stylets and into the gut lumen within the aphid. Subsequently, virions traverse the lining of the midgut, hindgut, or both (7,8,25) and are released into the body cavity (hemocoel) to circulate in the hemolymph. Virions suspended in hemolymph that contact the paired accessory salivary glands (ASG) are actively transported by endocytosis into the ASG cells and then transported into the salivary duct to be transmitted into potential host plants. Interestingly, each luteovirid species is transmitted most efficiently only by a specific set of aphid species or populations within an aphid species, thus demonstrating a high level of vector specificity. The cellular mechanisms responsible for vector specificity are regulated by distinct interactions between the two virus structural proteins and unknown proteins in the aphid (12).The discovery of Gildow and Rochow (9) that competition occurred between se...

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Biomarker discovery from the top down: Protein biomarkers for efficient virus transmission by insects (Homoptera: Aphididae) discovered by coupling genetics and 2‐D DIGE

et al. 2011

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Yellow dwarf viruses cause the most economically important virus diseases of cereal crops worldwide and are vectored by aphids. The identification of vector proteins mediating virus transmission is critical to develop sustainable virus management practices and to understand viral strategies for circulative movement in all insect vectors. Previously, we applied 2-D DIGE to an aphid filial generation 2 population to identify proteins correlated with the transmission phenotype that were stably inherited and expressed in the absence of the virus. In the present study, we examined the expression of the DIGE candidates in previously unstudied, field-collected aphid populations. We hypothesized that the expression of proteins involved in virus transmission could be clinically validated in unrelated, virus transmission-competent, field-collected aphid populations. All putative biomarkers were expressed in the field-collected biotypes, and the expression of nine of these aligned with the virus transmission-competent phenotype. The strong conservation of the expression of the biomarkers in multiple field-collected populations facilitates new and testable hypotheses concerning the genetics and biochemistry of virus transmission. Integration of these biomarkers into current aphid-scouting methodologies will enable rational strategies for vector control aimed at judicious use and development of precision pest control methods that reduce plant virus infection.

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Biometrical genetic analysis of luteovirus transmission in the aphid Schizaphis graminum

Cited by 31 publications

References 66 publications

Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission

Genetics Coupled to Quantitative Intact Proteomics Links Heritable Aphid and Endosymbiont Protein Expression to Circulative Polerovirus Transmission

Coupling Genetics and Proteomics To Identify Aphid Proteins Associated with Vector-Specific Transmission of Polerovirus ( Luteoviridae )

Biomarker discovery from the top down: Protein biomarkers for efficient virus transmission by insects (Homoptera: Aphididae) discovered by coupling genetics and 2‐D DIGE

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