Tangible benefits of the aphid Acyrthosiphon pisum genome sequencing for aphid proteomics: Enhancements in protein identification and data validation for homology-based proteomics

Cilia, Michelle; Tamborindeguy, Cécilia; Rolland, Mathieu; Howe, Kevin J.; Thannhauser, Theodore W.; Gray, Stewart M.

doi:10.1016/j.jinsphys.2010.11.001

Cited by 16 publications

(14 citation statements)

References 51 publications

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“…There is a paucity of tools to study vector biology and vectorvirus-host interactions at the molecular level; however, mass spectrometry technologies are emerging as one of the most powerful tools to develop a comprehensive understanding of virusvector-host interactions [9,18,22,77,78,79,80,81,82,83]. We used mass spectrometry to describe several host proteins that associate with virions and to show they may even be ingested by aphids during feeding.…”

Section: Discussionmentioning

confidence: 99%

“…Each unique peptide match is based on at least 2 distinct spectra, but in some cases, many more. In the case of cysteine-rich repeat secretory protein 55-like, more than 300 total spectra were matched, highlighting the limitations of a homology-based search strategy for protein identification [79]. doi:10.1371/journal.pone.0048177.t004…”

Section: Cydv-rpv-associated Host Proteins Accumulate Differentially mentioning

confidence: 99%

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Discovery and Targeted LC-MS/MS of Purified Polerovirus Reveals Differences in the Virus-Host Interactome Associated with Altered Aphid Transmission

et al. 2012

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Circulative transmission of viruses in the Luteoviridae, such as cereal yellow dwarf virus (CYDV), requires a series of precisely orchestrated interactions between virus, plant, and aphid proteins. Natural selection has favored these viruses to be retained in the phloem to facilitate acquisition and transmission by aphids. We show that treatment of infected oat tissue homogenate with sodium sulfite reduces transmission of the purified virus by aphids. Transmission electron microscopy data indicated no gross change in virion morphology due to treatments. However, treated virions were not acquired by aphids through the hindgut epithelial cells and were not transmitted when injected directly into the hemocoel. Analysis of virus preparations using nanoflow liquid chromatography coupled to tandem mass spectrometry revealed a number of host plant proteins co-purifying with viruses, some of which were lost following sodium sulfite treatment. Using targeted mass spectrometry, we show data suggesting that several of the virus-associated host plant proteins accumulated to higher levels in aphids that were fed on CYDV-infected plants compared to healthy plants. We propose two hypotheses to explain these observations, and these are not mutually exclusive: (a) that sodium sulfite treatment disrupts critical virion-host protein interactions required for aphid transmission, or (b) that host infection with CYDV modulates phloem protein expression in a way that is favorable for virus uptake by aphids. Importantly, the genes coding for the plant proteins associated with virus may be examined as targets in breeding cereal crops for new modes of virus resistance that disrupt phloem-virus or aphid-virus interactions.

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Section: Discussionmentioning

confidence: 99%

Section: Cydv-rpv-associated Host Proteins Accumulate Differentially mentioning

confidence: 99%

Discovery and Targeted LC-MS/MS of Purified Polerovirus Reveals Differences in the Virus-Host Interactome Associated with Altered Aphid Transmission

et al. 2012

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“…However, MALDI-MS/MS is known to identify the most prevalent protein present in a gel spot sample (Jun et al, 2012), and the top-ranked hit resulting from LC-MS/MS analysis has also been shown typically to correspond to the most abundant protein among multiple proteins present in a spot (Yang et al, 2007). The spot intensities of different protein constituents were determined using the protein abundance index and the exponentially modified protein abundance index (emPAI; Supplemental Table S3), which have been routinely applied in proteomics workflows (Perkins et al, 1999;Ishihama et al, 2005;Zhang et al, 2006;Yang et al, 2007;Cilia et al, 2011;Taylor et al, 2011). In this study, if more than one protein was identified in a spot, the relative abundance of each protein was determined by calculating the emPAI from the MS/MS data, and the assumption was made that the most abundant protein would account for the observed regulation (Ishihama et al, 2005).…”

Section: Proteomic Changes In Low-oxalate Transgenic Fruitmentioning

confidence: 99%

Reduction of Oxalate Levels in Tomato Fruit and Consequent Metabolic Remodeling Following Overexpression of a Fungal Oxalate Decarboxylase

Chakraborty

Ghosh

et al. 2013

Plant Physiology

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The plant metabolite oxalic acid is increasingly recognized as a food toxin with negative effects on human nutrition. Decarboxylative degradation of oxalic acid is catalyzed, in a substrate-specific reaction, by oxalate decarboxylase (OXDC), forming formic acid and carbon dioxide. Attempts to date to reduce oxalic acid levels and to understand the biological significance of OXDC in crop plants have met with little success. To investigate the role of OXDC and the metabolic consequences of oxalate down-regulation in a heterotrophic, oxalic acid-accumulating fruit, we generated transgenic tomato (Solanum lycopersicum) plants expressing an OXDC (FvOXDC) from the fungus Flammulina velutipes specifically in the fruit. These E8.2-OXDC fruit showed up to a 90% reduction in oxalate content, which correlated with concomitant increases in calcium, iron, and citrate. Expression of OXDC affected neither carbon dioxide assimilation rates nor resulted in any detectable morphological differences in the transgenic plants. Comparative proteomic analysis suggested that metabolic remodeling was associated with the decrease in oxalate content in transgenic fruit. Examination of the E8.2-OXDC fruit proteome revealed that OXDC-responsive proteins involved in metabolism and stress responses represented the most substantially up-and down-regulated categories, respectively, in the transgenic fruit, compared with those of wild-type plants. Collectively, our study provides insights into OXDC-regulated metabolic networks and may provide a widely applicable strategy for enhancing crop nutritional value.

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“…In the present study, we coupled two-dimensional (2-D) fluorescence difference gel electrophoresis (DIGE), one of the most widely used platforms for quantitative proteomics (68), and tandem mass spectrometry with genetic analyses to quantitatively compare the proteomes of S. graminum genotypes that differ in the ability to transmit CYDV-RPV. The recently published genome sequence of the aphid species A. pisum has provided additional resources for protein discovery in our S. graminum genotypes and has propelled proteomics to the forefront of biological discovery technologies for S. graminum and other aphid species (10,14,25,26,50,51,74).…”

mentioning

confidence: 99%

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

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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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Tangible benefits of the aphid Acyrthosiphon pisum genome sequencing for aphid proteomics: Enhancements in protein identification and data validation for homology-based proteomics

Cited by 16 publications

References 51 publications

Discovery and Targeted LC-MS/MS of Purified Polerovirus Reveals Differences in the Virus-Host Interactome Associated with Altered Aphid Transmission

Discovery and Targeted LC-MS/MS of Purified Polerovirus Reveals Differences in the Virus-Host Interactome Associated with Altered Aphid Transmission

Reduction of Oxalate Levels in Tomato Fruit and Consequent Metabolic Remodeling Following Overexpression of a Fungal Oxalate Decarboxylase

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

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