Metabolomics,Unknown,Transcriptomics,Genomics,Proteomics

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Characterization of Arabidopsis transcriptome responses to different aphid species reveals genes that contribute to host susceptibility and nonhost resistance

ABSTRACT: Background: Aphids are economically important pests and that display exceptional variation in host range. The underlying mechanism of diverse aphid host ranges are not well understood, but it is likely that molecular interactions are involved. With significant progress being made towards understanding host responses upon aphid attack, the mechanisms underlying nonhost resistance remain to be elucidated. Here, we investigated and compared Arabidopsis host and nonhost responses to aphids at the transcriptome level using three different aphid species. Results: Gene expression analyses revealed a surprising level of overlap in the overall gene expression changes during host and nonhost interactions with regards to the sets of genes differentially expressed and the direction of expression changes. Despite the overlap in transcriptional responses across interactions, there was a stronger repression of genes involved in metabolism and oxidative responses specifically during the host interaction. In addition we indentified a set of genes with opposite gene expression patterns during host versus nonhost interactions. Aphid performance assays on Arabidopsis mutants selected based on our transcriptome analyses identified genes involved in host and nonhost interactions. Conclusions: Understanding how plants respond to aphid species that differ in their ability to infest plant species, and identifying the genes and signaling pathways involved, is essential for the development of novel and durable aphid control in crop plants. Our work is an important step forward to provide such essential insights in that we identified novel genes contributing to host susceptibility, host defences as well nonhost resistance to aphids.

INSTRUMENT(S): Agilent Technologies G2505B scanner

ORGANISM(S): Arabidopsis thaliana

SUBMITTER: Pete Hedley

PROVIDER: E-MTAB-3223 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Project description:In most aphid species, facultative parthenogenetic reproduction allows rapid growth and formation of large single-genotype colonies. Upon predator attack, individual aphids emit an alarm pheromone to warn the colony of this danger. (E)-beta-farnesene (EBF) is the predominant constituent of the alarm pheromone in Myzus persicae (green peach aphid) and many other aphid species. Continuous exposure to alarm pheromone in aphid colonies raised on transgenic Arabidopsis thaliana plants that produce EBF leads to habituation of the aphid population. Whereas naïve aphids are repelled by EBF, habituated aphids show no avoidance response. Individual aphids from the habituated colony can revert back to being EBF-sensitive in three generations, indicating that this behavioral change is not caused by a genetic mutation. Instead, DNA microarray experiments comparing gene expression in naïve and habituated aphids treated with EBF demonstrate an almost complete desensitization in the transcriptional response to EBF. Furthermore, EBF-responsive aphids, but not habituated aphids show significantly lower reproduction in the presence of EBF. Although both naïve and habituated aphids emit EBF upon damage, EBF-responsive aphids display a higher survival rate in the presence of coccinellid predators and thus outperform habituated aphids that do not show an avoidance response. These results provide direct evidence that aphid perception of conspecific alarm pheromone aids in predator avoidance and thereby bestows fitness benefits in survivorship and fecundity. Although habituated M. persicae have equal fecundity on control and EBF-producing plants, such transgenics may have practical applications in agriculture because of increased predation of habituated aphids. Log fold-changes (LogFC) were computed and contigs with P-values ≤ 0.05 were considered to be differentially expressed (see Supplementary file at foot of this record). Agilent 8x15K array previously reported by Ramsey et al., 2007 - BMC Genomics 8: 243. Two-condition experiment using Alexa Fluor 555 and 647 dyes. Biological replicates: 4 control replicates, 4 treated replicates.

Project description:Aphids, sap-sucking insects in the order Hemiptera, are among the most prolific insect vectors of plant viruses Plant viruses from the family Luteoviridae are transmitted exclusively by aphids in a circulative manner and cause significant crop yield losses. Circulative plant viruses must cross the aphid gut and other tissues prior to transmission to a new host plant. The discovery of proteins that control acquisition and transmission in the insect vector is the biggest challenge for the vector biology field and will have practical applications for growers by providing new molecular targets for the development of precision vector management tools. The green peach aphid, Myzus persicae, is a vector of the Potato leafroll virus (PLRV), a polerovirus in the Luteoviridae. PLRV transmission efficiency was significantly reduced when a clonal lineage of M. persicae was reared on turnip (T-Myzus) as compared to the weed physalis (P-Myzus). The effect on PLRV transmission efficiency was transient and caused by a host-switch response. Using 2-D DIGE, we revealed that the major difference in the proteome profile of P- and T-Myzus was the lysosomal cysteine protease cathepsin B, with multiple size and charge isoforms of this enzyme up-regulated in T-Myzus. Quantitative, shotgun proteomics revealed a specific upregulation in the expression of other lysosomal proteins in T-Myzus as compared to P-Myzus, including cathepsin B, cathepsin B-16, beta-glucuronidase, peroxidasin, legumain-like, and aminopeptidase-N. The titer of PLRV was over 1.5 fold higher in P-Myzus than in T-Myzus at 24h and 72h after the beginning of virus acquisition, suggesting that virus acquisition in P-Myzus was more efficient. Cathepsin B and PLRV localization were starkly different in P- and T-Myzus midguts, the site of PLRV acquisition into the insect. In P-Myzus midguts, an abundance of PLRV was observed inside midgut cells, and cathepsin B was sequestered in a subcellular compartment. In contrast, there is near complete co-localization of cathepsin B and PLRV at the cell membranes in viruliferous T-Myzus. Inhibition of cathepsin and other cysteine proteases with E64 restored the ability of T-Myzus to transmit PLRV in a dose-dependent manner, suggesting that the activities of lysosomal cysteine proteases at the cell membrane in T-Myzus is responsible for the change in virus transmission phenotype in these aphids. T-Myzus individuals weighed more and had more progeny than P-Myzus individuals. These data are all consistent with the hypothesis that there is an induction of lysosomal exocytos in the midgut of T-Myzus linked to the ability of the aphid to acquire PLRV. These data also show that the ability of the generalist aphid M. persicae to transmit PLRV is influenced by the host plant the aphids are reared on, information that is useful to growers for polerovirus management in field crops.

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Characterization of Arabidopsis transcriptome responses to different aphid species reveals genes that contribute to host susceptibility and nonhost resistance

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